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Ovarian expression of Insulin-Like peptide 3 (INSL3) and its receptor (RXFP2) during development of bovine antral follicles and corpora lutea and measurement of circulating INSL3 levels during synchronized estrous cycles

Satchell, Leanne; Glister, Claire; Bleach, Emma C.; Glencross, Richard G.; Bicknell, Andrew B.; Dai, Yanzhenzi; Anand-Ivell, Ravinder; Ivell, Richard; Knight, Philip G.

Authors

Leanne Satchell

Claire Glister

Emma C. Bleach

Richard G. Glencross

Andrew B. Bicknell

Yanzhenzi Dai

Ravinder Anand-Ivell ravinder.anand-ivell@nottingham.ac.uk

Richard Ivell richard.ivell@nottingham.ac.uk

Philip G. Knight



Abstract

Insulin-like peptide 3 (INSL3), a major product of testicular Leydig cells, is also expressed by the ovary, but its functional role remains poorly understood. Here, we quantified expression of INSL3 and its receptor RXFP2 in theca interna cell (TIC) and granulosa cell compartments of developing bovine antral follicles and in corpora lutea (CL). INSL3 and RXFP2 mRNA levels were much higher in TIC than granulosa cellandincreased progressively during follicle maturation with INSL3 peaking in large (11-18 mm) estrogen-active follicles and RXFP2 peaking in 9- to 10-mm follicles before declining in larger (11-18 mm) follicles. Expression of both INSL3 and RXFP2 in CL was much lower than in TIC. In situ hybridization and immunohistochemistry confirmed abundant expression of INSL3 mRNA and protein in TIC. These observations indicate follicular TIC rather than CL as the primary site of both INSL3 production and action, implying a predominantly autocrine/paracrine role in TIC. To corroborate the above findings, we showed that in vitro exposure of TIC to a luteinizing concentration of LH greatly attenuated expression of both INSL3 and its receptor while increasing progesterone secretion and expression of STAR and CYP11A1. Moreover, in vivo, a significant cyclic variation in plasma INSL3 was observed during synchronized estrous cycles. INSL3 and estradiol-17beta followed a similar pattern, both increasing after luteolysis, before falling sharply after the LH surge. Thus, theca-derived INSL3, likely from the dominant preovulatory follicle, is detectable in peripheral blood of cattle, and expression is down-regulated during luteinization induced by the preovulatory LH surge. Collectively, these findings underscore the likely role of INSL3 as an important intrafollicular modulator of TIC function/steroidogenesis, while raising doubts about its potential contribution to CL function.

Journal Article Type Article
Publication Date May 1, 2013
Journal Endocrinology
Print ISSN 0013-7227
Electronic ISSN 1945-7170
Publisher Oxford University Press (OUP)
Peer Reviewed Peer Reviewed
Volume 154
Issue 5
Institution Citation Satchell, L., Glister, C., Bleach, E. C., Glencross, R. G., Bicknell, A. B., Dai, Y., …Knight, P. G. (2013). Ovarian expression of Insulin-Like peptide 3 (INSL3) and its receptor (RXFP2) during development of bovine antral follicles and corpora lutea and measurement of circulating INSL3 levels during synchronized estrous cycles. Endocrinology, 154(5), doi:10.1210/en.2012-2232
DOI https://doi.org/10.1210/en.2012-2232
Keywords in situ hybridization immunohistochemistry estrogen cattle cholesterol monooxygenase (side-chain-cleaving) corpus luteum of ovary estrous cycle granulosa cell hair follicle interstitial cell of leydig ovarian follicle peptides plasma rna, messenger insuli
Publisher URL https://academic.oup.com/endo/article-lookup/doi/10.1210/en.2012-2232
Copyright Statement Copyright information regarding this work can be found at the following address: http://eprints.nottingh.../end_user_agreement.pdf

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Copyright Statement
Copyright information regarding this work can be found at the following address: http://eprints.nottingham.ac.uk/end_user_agreement.pdf





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