Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T07:44:15.077Z Has data issue: false hasContentIssue false
  • English
  • Français

A bovine-specific FSH enzyme immunoassay and its application to study the role of FSH in ovarian follicle development during the postnatal period

Published online by Cambridge University Press:  20 December 2018

A.-L. Lainé ,
C. Laclie ,
J. Furlong ,
M. A. Crowe  and
D. Monniaux Open the ORCID record for D. Monniaux [Opens in a new window]
A.-L. Lainé*
Affiliation:
UMR Physiologie de la Reproduction et des Comportements, INRA, CNRS, IFCE, Université de Tours, 37380 Nouzilly, France
C. Laclie
Affiliation:
UMR Physiologie de la Reproduction et des Comportements, INRA, CNRS, IFCE, Université de Tours, 37380 Nouzilly, France
J. Furlong
Affiliation:
UCD School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
M. A. Crowe
Affiliation:
UCD School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
D. Monniaux
Affiliation:
UMR Physiologie de la Reproduction et des Comportements, INRA, CNRS, IFCE, Université de Tours, 37380 Nouzilly, France
*
†E-mail: anne-lyse.laine@inra.fr
Get access

Abstract

The primary aim of this study was to develop a FSH enzyme immunoassay (EIA) for the bovine species. The newly developed EIA was validated for FSH determination in bovine plasma by comparison with an existing bovine FSH radioimmunoassay. The EIA detected bovine FSH with a high sensitivity (0.1 ng/ml). Cross-reactivity of the EIA was 0.01% with bovine LH, 51% with ovine FSH, <0.1% with porcine FSH and <0.01% with equine FSH. Using this EIA on different time series of plasma in cows, we have confirmed the presence of a FSH pre-ovulatory peak at estrus, of periodic FSH fluctuations accompanying the waves of terminal follicular development, and of FSH pulses, mainly asynchronous with LH ones, in the peri-ovulatory phase of the cycle. In a second objective, the EIA was used to assess the role of FSH in regulating the development of ovarian follicles up to the small antral stage in young calves. To answer this question, six calves were submitted to weekly blood sampling during their first 3 months of life, and FSH changes were studied concomitantly to those of anti-Müllerian hormone (AMH), a well-established endocrine marker of the ovarian population of small antral follicles in cows. In the ovaries of 3-month calves, the population of 3 to 5 mm follicles contained the highest intra-follicular AMH amounts, and the number of 3 to 5 mm follicles on ovaries was closely correlated with AMH concentrations in the plasma of calves at this age (rs = 0.94). Before 3 months of age, only two out of six calves showed a clear postnatal FSH peak in plasma, and no correlation was found between plasma FSH and AMH concentrations. These results indicate that female calves undergo different patterns of FSH secretion and that postnatal activation of follicular growth up to the small antral stage appears independent and not directly related to circulating FSH levels.

Keywords

FSHimmunoassayovarycowcalf
Type
Research Article
Information
animal , Volume 13 , Issue 8 , August 2019 , pp. 1666 - 1675
Copyright
© The Animal Consortium 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, GP, Jaiswal, R, Singh, J and Malhi, P 2008. Progress in understanding ovarian follicular dynamics in cattle. Theriogenology 69, 72–80.10.1016/j.theriogenology.2007.09.026Google Scholar
Boer, HMT, Butler, ST, Stotzel, C, Te Pas, MFW, Veerkamp, RF and Woelders, H 2017. Validation of a mathematical model of the bovine estrous cycle for cows with different estrous cycle characteristics. Animal 11, 1991–2001.10.1017/S175173111700026XGoogle Scholar
Burns, DS, Jimenez-Krassel, F, Ireland, JL, Knight, PG and Ireland, JJ 2005. 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. Biology of Reproduction 73, 54–62.10.1095/biolreprod.104.036277Google Scholar
Butler, ST, Pelton, SH, Knight, PG and Butler, WR 2008. Follicle-stimulating hormone isoforms and plasma concentrations of estradiol and inhibin A in dairy cows with ovulatory and non-ovulatory follicles during the first postpartum follicle wave. Domestic Animal Endocrinology 35, 112–119.10.1016/j.domaniend.2008.03.002Google Scholar
Canepa, S, Lainé, AL, Bluteau, A, Fagu, C, Flon, C and Monniaux, D 2008. Validation d’une méthode immunoenzymatique pour le dosage de la progestérone dans le plasma des ovins et des bovins. Cahier des Techniques de l’Inra 64, 19–30.Google Scholar
Clarke, I, Moore, L and Veldhuis, J 2002. Intensive direct cavernous sinus sampling identifies high-frequency, nearly random patterns of FSH secretion in ovariectomized ewes: combined appraisal by RIA and bioassay. Endocrinology 143, 117–129.10.1210/endo.143.1.8644Google Scholar
Combarnous, Y 1992. Molecular basis of the specificity of binding of glycoprotein hormones to their receptors. Endocrine Reviews 13, 670–691.10.1210/edrv-13-4-670Google Scholar
Cooke, DJ, Crowe, MA, Roche, JF and Headon, DR 1996. Gonadotrophin heterogeneity and its role in farm animal reproduction. Animal Reproduction Science 41, 77–99.10.1016/0378-4320(95)01449-7Google Scholar
Crowe, MA, Padmanabhan, V, Hynes, N, Sunderland, SJ, Enright, WJ, Beitins, IZ and Roche, JF 1997. Validation of a sensitive radioimmunoassay to measure serum follicle-stimulating hormone in cattle: correlation with biological activity. Animal Reproduction Science 48, 123–136.10.1016/S0378-4320(97)00022-5Google Scholar
Dhali, A, Mishra, DP, Karunakaran, M, Mech, A and Rajkhowa, C 2006. Secretion patterns of luteinising hormone, follicle-stimulating hormone and 17beta-oestradiol during oestrus and the mid-luteal phase of the oestrous cycle in mithun (Bos frontalis). Reproduction, Fertility and Development 18, 619–626.10.1071/RD06005Google Scholar
Dirnhofer, S, Lechner, O, Madersbacher, S, Klieber, R, de Leeuw, R, Wick, G and Berger, P 1994. Free alpha subunit of human chorionic gonadotrophin: molecular basis of immunologically and biologically active domains. Journal of Endocrinology 140, 145–154.10.1677/joe.0.1400145Google Scholar
Dodson, SE, McLeod, BJ, Haresign, W, Peters, AR and Lamming, GE 1988. Endocrine changes from birth to puberty in the heifer. Journal of Reproduction and Fertility 82, 527–538.10.1530/jrf.0.0820527Google Scholar
El-Sheikh Ali, H, Kitahara, G, Takahashi, T, Mido, S, Sadawy, M, Kobayashi, I, Hemmi, K and Osawa, T 2017. Plasma anti-Mullerian hormone profile in heifers from birth through puberty and relationship with puberty onset. Biology of Reproduction 97, 153–161.10.1093/biolre/iox069Google Scholar
Evans, AC, Adams, GP and Rawlings, NC 1994. Follicular and hormonal development in prepubertal heifers from 2 to 36 weeks of age. Journal of Reproduction and Fertility 102, 463–470.10.1530/jrf.0.1020463Google Scholar
Evans, AC, Currie, WD and Rawlings, NC 1992. Effects of naloxone on circulating gonadotrophin concentrations in prepubertal heifers. Journal of Reproduction and Fertility 96, 847–855.10.1530/jrf.0.0960847Google Scholar
Faure, MO, Nicol, L, Fabre, S, Fontaine, J, Mohoric, N, McNeilly, A and Taragnat, C 2005. BMP-4 inhibits follicle-stimulating hormone secretion in ewe pituitary. Journal of Endocrinology 186, 109–121.10.1677/joe.1.05988Google Scholar
Fortune, JE 1994. Ovarian follicular growth and development in mammals. Biology of Reproduction 50, 225–232.10.1095/biolreprod50.2.225Google Scholar
Fox, KM, Dias, JA and Van Roey, P 2001. Three-dimensional structure of human follicle-stimulating hormone. Molecular Endocrinology 15, 378–389.10.1210/mend.15.3.0603Google Scholar
Ginther, OJ 2016. The theory of follicle selection in cattle. Domestic Animal Endocrinology 57, 85–99.Google Scholar
Ginther, OJ, Siddiqui, MA, Baldrighi, JM, Wolf, CA and Castro, T 2016. Temporality of two-way functional coupling between FSH and follicles in heifers. Theriogenology 86, 1645–1653.10.1016/j.theriogenology.2015.10.006Google Scholar
Haj Hassan, M, Cahoreau, C, Jegot, G, Jouanny, C, Mariot, J, Lecompte, F, Klett, D and Combarnous, Y 2015. Differential thermal stability of human, bovine and ovine follicle-stimulating hormone (FSH) and luteinizing hormone (LH) quaternary structures. General and Comparative Endocrinology 212, 124–130.Google Scholar
Hillier, SG 2001. Gonadotropic control of ovarian follicular growth and development. Molecular and Cellular Endocrinology 179, 39–46.Google Scholar
Ireland, JJ, Mihm, M, Austin, E, Diskin, MG and Roche, JF 2000. Historical perspective of turnover of dominant follicles during the bovine estrous cycle: key concepts, studies, advancements, and terms. Journal of Dairy Science 83, 1648–1658.10.3168/jds.S0022-0302(00)75033-8Google Scholar
Kaneko, H, Noguchi, J, Kikuchi, K, Akagi, S, Shimada, A, Taya, K, Watanabe, G and Hasegawa, Y 2001. Production and endocrine role of inhibin during the early development of bull calves. Biology of Reproduction 65, 209–215.10.1095/biolreprod65.1.209Google Scholar
Lussier, JG, Matton, P and Dufour, JJ 1987. Growth rates of follicles in the ovary of the cow. Journal of Reproduction and Fertility 81, 301–307.10.1530/jrf.0.0810301Google Scholar
McGee, EA and Hsueh, AJ 2000. Initial and cyclic recruitment of ovarian follicles. Endocrine Reviews 21, 200–214.Google Scholar
McNeilly, AS, Crawford, JL, Taragnat, C, Nicol, L and McNeilly, JR 2003. The differential secretion of FSH and LH: regulation through genes, feedback and packaging. Reproduction (Cambridge, England) (suppl. 61), 463–476.Google Scholar
Monniaux, D, Clément, F, Dalbies-Tran, R, Estienne, A, Fabre, S, Mansanet, C and Monget, P 2014. The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link? Biology of Reproduction 90, 85.Google Scholar
Monniaux, D, Drouilhet, L, Rico, C, Estienne, A, Jarrier, P, Touzé, JL, Sapa, J, Phocas, F, Dupont, J, Dalbies-Tran, R and Fabre, S 2013. Regulation of anti-Mullerian hormone production in domestic animals. Reproduction, Fertility and Development 25, 1–16.Google Scholar
Padmanabhan, V and Sharma, TP 2001. Neuroendocrine vs. paracrine control of follicle-stimulating hormone. Archives of Medical Research 32, 533–543.10.1016/S0188-4409(01)00318-6Google Scholar
Rawlings, NC, Evans, AC, Honaramooz, A and Bartlewski, PM 2003. Antral follicle growth and endocrine changes in prepubertal cattle, sheep and goats. Animal Reproduction Science 78, 259–270.Google Scholar
Rhodes, FM, Fitzpatrick, LA, Entwistle, KW and Kinder, JE 1995. Hormone concentrations in the caudal vena cava during the first ovarian follicular wave of the oestrous cycle in heifers. Journal of Reproduction and Fertility 104, 33–39.Google Scholar
Richards, JS 1994. Hormonal control of gene expression in the ovary. Endocrine Reviews 15, 725–751.Google Scholar
Rico, C, Drouilhet, L, Salvetti, P, Dalbies-Tran, R, Jarrier, P, Touzé, JL, Pillet, E, Ponsart, C, Fabre, S and Monniaux, D 2012. Determination of anti-Mullerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm. Reproduction, Fertility and Development 24, 932–944.10.1071/RD11290Google Scholar
Rico, C, Médigue, C, Fabre, S, Jarrier, P, Bontoux, M, Clément, F and Monniaux, D 2011. Regulation of anti-Mullerian hormone production in the cow: a multiscale study at endocrine, ovarian, follicular, and granulosa cell levels. Biology of Reproduction 84, 560–571.Google Scholar
Scaramuzzi, RJ, Baird, DT, Campbell, BK, Driancourt, MA, Dupont, J, Fortune, JE, Gilchrist, RB, Martin, GB, McNatty, KP, McNeilly, AS, Monget, P, Monniaux, D, Vinoles, C and Webb, R 2011. Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reproduction, Fertility and Development 23, 444–467.Google Scholar
Tanaka, Y, Nakada, K, Moriyoshi, M and Sawamukai, Y 2001. Appearance and number of follicles and change in the concentration of serum FSH in female bovine fetuses. Reproduction 121, 777–782.Google Scholar
Thompson, IR and Kaiser, UB 2014. GnRH pulse frequency-dependent differential regulation of LH and FSH gene expression. Molecular and Cellular Endocrinology 385, 28–35.10.1016/j.mce.2013.09.012Google Scholar
Torres-Rovira, L, Succu, S, Pasciu, V, Manca, ME, Gonzalez-Bulnes, A, Leoni, GG, Pennino, MG, Spezzigu, A, Gallus, M, Dattena, M, Monniaux, D, Naitana, S and Berlinguer, F 2016. Postnatal pituitary and follicular activation: a revisited hypothesis in a sheep model. Reproduction 151, 215–225.Google Scholar
Ulloa-Aguirre, A, Timossi, C, Barrios-de-Tomasi, J, Maldonado, A and Nayudu, P 2003. Impact of carbohydrate heterogeneity in function of follicle-stimulating hormone: studies derived from in vitro and in vivo models. Biology of Reproduction 69, 379–389.10.1095/biolreprod.103.016915Google Scholar
Vidal, A, Zhang, Q, Medigue, C, Fabre, S and Clement, F 2012. DynPeak: an algorithm for pulse detection and frequency analysis in hormonal time series. PLoS One 7, e39001.10.1371/journal.pone.0039001Google Scholar
Walters, DL and Schallenberger, E 1984. Pulsatile secretion of gonadotrophins, ovarian steroids and ovarian oxytocin during the periovulatory phase of the oestrous cycle in the cow. Journal of Reproduction and Fertility 71, 503–512.10.1530/jrf.0.0710503Google Scholar
Wandji, SA, Pelletier, G and Sirard, MA 1992. Ontogeny and cellular localization of 125I-labeled insulin-like growth factor-I, 125I-labeled follicle-stimulating hormone, and 125I-labeled human chorionic gonadotropin binding sites in ovaries from bovine fetuses and neonatal calves. Biology of Reproduction 47, 814–822.Google Scholar
Yang, MY and Fortune, JE 2008. The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biology of Reproduction 78, 1153–1161.Google Scholar