Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2016

Open Access 01-12-2016 | Research

ACTH-induced stress in weaned sows impairs LH receptor expression and steroidogenesis capacity in the ovary

Authors: H. S. Zhu, Z. Qian, H. L. Liu, E. D. Bao

Published in: Reproductive Biology and Endocrinology | Issue 1/2016

Login to get access

Abstract

Background

Stress has been proved to impair the porcine reproduction soundly. Endocrine disruption, which is closely related to the persistent follicles, is possibly one of the results of stress, although the mechanism is unclear. Since the expression of luteinizing hormone receptor (LHR) in ovarian follicular wall and concentrations of steroid hormone in follicular fluid are related to the development of persistent follicles, this study is designed to evaluate the effect of administered adrenocorticotrophic hormone (ACTH) to weaned pigs on their ovarian steroidogenesis capacity and LHR expression.

Methods

Ten multiparous sows were weaned and randomly divided into two groups (n = 5 each). Sows received 1 IU/kg ACTH (ACTH group) or saline (control group) every 8 h from days 3–9 after jugular vein intubation. Blood samples were collected throughout the experiment, and ovaries were collected after slaughter on day 10. Follicular fluid (FF) was used to determine the steroid hormone concentrations. The ovarian follicle wall was obtained and stored in liquid nitrogen to detect mRNA levels.

Results

The plasma cortisol concentration was significantly (P < 0.01) elevated after ACTH injection. The estradiol (E2) and androstenedione (ASD) concentrations in FF were significantly lower (P < 0.05) in the ACTH group than in the control group. The LHR, 3β-hydroxysteroid dehydrogenase (3β-HSD), cytochrome P450 aromatase (P450arom), and cytochrome P450 17a-hydroxylase (P450c17) mRNA levels were significantly (P < 0.05) reduced in the ACTH group. The steroidogenic acute regulatory protein (StAR) level and cytochrome P450 side-chain cleavage (P450scc) was lower in the ACTH group than in the control group, but the difference was not statistically significant (P > 0.05). Immunostaining results revealed 3β-HSD,P450c17, and LHR expression in theca cells, and P450arom expression in granulosa cells. Immunohistochemical staining showed significant differences in the distribution of 3β-HSD, P450c17, LHR, and P450arom between the two groups.

Conclusions

These findings indicated that ACTH significantly diminished the LHR expression and steroidogenesis capacity of the ovaries of weaned sows.
Literature
1.
go back to reference Dobson H, Smith RF. What is stress, and how does it affect reproduction? Anim Reprod Sci. 2000;60–61:743–52.CrossRefPubMed Dobson H, Smith RF. What is stress, and how does it affect reproduction? Anim Reprod Sci. 2000;60–61:743–52.CrossRefPubMed
3.
go back to reference Wingfield JC, Sapolsky RM. Reproduction and resistance to stress: When and how. J Neuroendocrinol. 2003;15:711–24.CrossRefPubMed Wingfield JC, Sapolsky RM. Reproduction and resistance to stress: When and how. J Neuroendocrinol. 2003;15:711–24.CrossRefPubMed
4.
go back to reference Castagna CD, Peixoto CH, Bortolozzo FP, Wentz I, Neto GB, Ruschel FC. Ovarian cysts and their consequences on the reproductive performance of swine herds. Anim Reprod Sci. 2004;81:115–23.CrossRefPubMed Castagna CD, Peixoto CH, Bortolozzo FP, Wentz I, Neto GB, Ruschel FC. Ovarian cysts and their consequences on the reproductive performance of swine herds. Anim Reprod Sci. 2004;81:115–23.CrossRefPubMed
5.
go back to reference Szulanczyk-Mencel K, Rzasa A, Bielas W. Relationships between ovarian cysts and morphological and hormonal state of ovarian cortex in sows. Anim Reprod Sci. 2010;121:273–8.CrossRefPubMed Szulanczyk-Mencel K, Rzasa A, Bielas W. Relationships between ovarian cysts and morphological and hormonal state of ovarian cortex in sows. Anim Reprod Sci. 2010;121:273–8.CrossRefPubMed
6.
go back to reference Hamilton SA, Garverick HA, Keisler DH, Xu ZZ, Loos K, Youngquist RS, Salfen BE. Characterization of ovarian follicular cysts and associated endocrine profiles in dairy cows. Biol Reprod. 1995;53:890–8.CrossRefPubMed Hamilton SA, Garverick HA, Keisler DH, Xu ZZ, Loos K, Youngquist RS, Salfen BE. Characterization of ovarian follicular cysts and associated endocrine profiles in dairy cows. Biol Reprod. 1995;53:890–8.CrossRefPubMed
7.
go back to reference Prunier A, Quesnel H. Nutritional influences on the hormonal control of reproduction in female pigs. Livest Prod Sci. 2000;63:1–16.CrossRef Prunier A, Quesnel H. Nutritional influences on the hormonal control of reproduction in female pigs. Livest Prod Sci. 2000;63:1–16.CrossRef
8.
go back to reference Brandt Y, Lang A, Madej A, Rodriguez-Martinez H, Einarsson S. Impact of ACTH administration on the oviductal sperm reservoir in sows: the local endocrine environment and distribution of spermatozoa. Anim Reprod Sci. 2006;92:107–22.CrossRefPubMed Brandt Y, Lang A, Madej A, Rodriguez-Martinez H, Einarsson S. Impact of ACTH administration on the oviductal sperm reservoir in sows: the local endocrine environment and distribution of spermatozoa. Anim Reprod Sci. 2006;92:107–22.CrossRefPubMed
9.
go back to reference Hennessy DP, Williamson P. The effects of stress and of ACTH administration in hormone profiles, oestrus and ovulation in pigs. Theriogenology. 1983;20:13–26.CrossRefPubMed Hennessy DP, Williamson P. The effects of stress and of ACTH administration in hormone profiles, oestrus and ovulation in pigs. Theriogenology. 1983;20:13–26.CrossRefPubMed
10.
go back to reference Ribadu AY, Nakada K, Moriyoshi M, Zhang WC, Tanaka Y, Nakao T. The role of LH pulse frequency in ACTH-induced ovarian follicular cysts in heifers. Anim Reprod Sci. 2000;64:21–31.CrossRefPubMed Ribadu AY, Nakada K, Moriyoshi M, Zhang WC, Tanaka Y, Nakao T. The role of LH pulse frequency in ACTH-induced ovarian follicular cysts in heifers. Anim Reprod Sci. 2000;64:21–31.CrossRefPubMed
11.
go back to reference Razdan P, Mwanza AM, Kindahl H, Rodriguez-Martinez H, Hulten F, Einarsson S. Effect of repeated ACTH-stimulation on early embryonic development and hormonal profiles in sows. Anim Reprod Sci. 2002;70:127–37.CrossRefPubMed Razdan P, Mwanza AM, Kindahl H, Rodriguez-Martinez H, Hulten F, Einarsson S. Effect of repeated ACTH-stimulation on early embryonic development and hormonal profiles in sows. Anim Reprod Sci. 2002;70:127–37.CrossRefPubMed
12.
go back to reference Madej A, Lang A, Brandt Y, Kindahl H, Madsen MT, Einarsson S. Factors regulating ovarian function in pigs. Domest Anim Endocr. 2005;29:347–61.CrossRef Madej A, Lang A, Brandt Y, Kindahl H, Madsen MT, Einarsson S. Factors regulating ovarian function in pigs. Domest Anim Endocr. 2005;29:347–61.CrossRef
13.
go back to reference Brandt Y, Lundeheim N, Madej A, Rodriguez-Martinez H, Einarsson S. Effects of ACTH injections during estrus on concentrations and patterns of progesterone, estradiol, LH, and inhibin alpha and time of ovulation in the sow. Domest Anim Endocr. 2007;32:122–37.CrossRef Brandt Y, Lundeheim N, Madej A, Rodriguez-Martinez H, Einarsson S. Effects of ACTH injections during estrus on concentrations and patterns of progesterone, estradiol, LH, and inhibin alpha and time of ovulation in the sow. Domest Anim Endocr. 2007;32:122–37.CrossRef
14.
go back to reference Vänttinen T, Kuulasmaa T, Liu J, Voutilainen R. Expression of Activin/Inhibin Receptor and Binding Protein Genes and Regulation of Activin/Inhibin Peptide Secretion in Human Adrenocortical Cells. J Clin Endocr Metab. 2002;87:4257–63.CrossRefPubMed Vänttinen T, Kuulasmaa T, Liu J, Voutilainen R. Expression of Activin/Inhibin Receptor and Binding Protein Genes and Regulation of Activin/Inhibin Peptide Secretion in Human Adrenocortical Cells. J Clin Endocr Metab. 2002;87:4257–63.CrossRefPubMed
15.
go back to reference Schams D, Berisha B. Steroids as local regulators of ovarian activity in domestic animals. Domest Anim Endocr. 2002;23:53–65.CrossRef Schams D, Berisha B. Steroids as local regulators of ovarian activity in domestic animals. Domest Anim Endocr. 2002;23:53–65.CrossRef
16.
go back to reference Guthrie HD, Cooper BS, Welch GR, Zakaria AD, Johnson LA. Atresia in Follicles Grown after Ovulation in the Pig: Measurement of Increased Apoptosis in Granulosa Cells and Reduced Follicular- Fluid Estradiol-17-Beta. Biol Reprod. 1995;52:920–7.CrossRefPubMed Guthrie HD, Cooper BS, Welch GR, Zakaria AD, Johnson LA. Atresia in Follicles Grown after Ovulation in the Pig: Measurement of Increased Apoptosis in Granulosa Cells and Reduced Follicular- Fluid Estradiol-17-Beta. Biol Reprod. 1995;52:920–7.CrossRefPubMed
17.
go back to reference Barb CR, Kraeling RR, Rampacek GB, Fonda ES, Kiser TE. Inhibition of ovulation and LH secretion in the gilt after treatment with ACTH or hydrocortisone. J Reprod Fertil. 1982;64:85–92.CrossRefPubMed Barb CR, Kraeling RR, Rampacek GB, Fonda ES, Kiser TE. Inhibition of ovulation and LH secretion in the gilt after treatment with ACTH or hydrocortisone. J Reprod Fertil. 1982;64:85–92.CrossRefPubMed
18.
go back to reference Ortega I, Villanueva JA, Wong DH, Cress AB, Sokalska A, Stanley SD, Duleba AJ. Resveratrol potentiates effects of simvastatin on inhibition of rat ovarian theca-interstitial cells steroidogenesis. J Ovarian Res. 2014;7:21.CrossRefPubMedPubMedCentral Ortega I, Villanueva JA, Wong DH, Cress AB, Sokalska A, Stanley SD, Duleba AJ. Resveratrol potentiates effects of simvastatin on inhibition of rat ovarian theca-interstitial cells steroidogenesis. J Ovarian Res. 2014;7:21.CrossRefPubMedPubMedCentral
19.
go back to reference Gregoraszczuk EL, Rak-Mardyla A. Supraphysiological leptin levels shift the profile of steroidogenesis in porcine ovarian follicles toward progesterone and testosterone secretion through increased expressions of CYP11A1 and 17 -HSD: a tissue culture approach. Reproduction. 2013;145:311–7.CrossRefPubMed Gregoraszczuk EL, Rak-Mardyla A. Supraphysiological leptin levels shift the profile of steroidogenesis in porcine ovarian follicles toward progesterone and testosterone secretion through increased expressions of CYP11A1 and 17 -HSD: a tissue culture approach. Reproduction. 2013;145:311–7.CrossRefPubMed
20.
go back to reference Mankiewicz JL, Godwin J, Holler BL, Turner PM, Murashige R, Shamey R, Daniels HV, Borski RJ. Masculinizing effect of background color and cortisol in a flatfish with environmental sex-determination. Integr Comp Biol. 2013;53:755–65.CrossRefPubMed Mankiewicz JL, Godwin J, Holler BL, Turner PM, Murashige R, Shamey R, Daniels HV, Borski RJ. Masculinizing effect of background color and cortisol in a flatfish with environmental sex-determination. Integr Comp Biol. 2013;53:755–65.CrossRefPubMed
21.
go back to reference Evans NP, Dahl GE, Mauger D, Karsch FJ. Estradiol Induces Both Qualitative and Quantitative Changes in the Pattern of Gonadotropin-Releasing-Hormone Secretion during the Presurge Period in the Ewe. Endocrinology. 1995;136:1603–9.PubMed Evans NP, Dahl GE, Mauger D, Karsch FJ. Estradiol Induces Both Qualitative and Quantitative Changes in the Pattern of Gonadotropin-Releasing-Hormone Secretion during the Presurge Period in the Ewe. Endocrinology. 1995;136:1603–9.PubMed
22.
go back to reference Lei ZM, Rao CV. Neural actions of luteinizing hormone and human chorionic gonadotropin. Semin Reprod Med. 2001;19:103–9.CrossRefPubMed Lei ZM, Rao CV. Neural actions of luteinizing hormone and human chorionic gonadotropin. Semin Reprod Med. 2001;19:103–9.CrossRefPubMed
23.
go back to reference Larzul C, Terenina E, Foury A, Billon Y, Louveau I, Merlot E, Mormede P. The cortisol response to ACTH in pigs, heritability and influence of corticosteroid-binding globulin. Animal. 2015;9:1929–34.CrossRefPubMed Larzul C, Terenina E, Foury A, Billon Y, Louveau I, Merlot E, Mormede P. The cortisol response to ACTH in pigs, heritability and influence of corticosteroid-binding globulin. Animal. 2015;9:1929–34.CrossRefPubMed
24.
go back to reference Scholten JA, Liptrap RM. A role for the adrenal cortex in the onset of cystic ovarian follicles in the sow. Can J Comp Med. 1978;42:525–33.PubMedPubMedCentral Scholten JA, Liptrap RM. A role for the adrenal cortex in the onset of cystic ovarian follicles in the sow. Can J Comp Med. 1978;42:525–33.PubMedPubMedCentral
25.
go back to reference Lang A, Kaeoket K, Kindahl H, Madej A, Einarsson S. Influence of CRH and ACTH administration on endocrine profile and ovulation in sows. Reprod Domest Anim. 2004;39:181–9.CrossRefPubMed Lang A, Kaeoket K, Kindahl H, Madej A, Einarsson S. Influence of CRH and ACTH administration on endocrine profile and ovulation in sows. Reprod Domest Anim. 2004;39:181–9.CrossRefPubMed
26.
go back to reference Aluru N, Vijayan MM. Aryl hydrocarbon receptor activation impairs cortisol response to stress in rainbow trout by disrupting the rate-limiting steps in steroidogenesis. Endocrinology. 2006;147:1895–903.CrossRefPubMed Aluru N, Vijayan MM. Aryl hydrocarbon receptor activation impairs cortisol response to stress in rainbow trout by disrupting the rate-limiting steps in steroidogenesis. Endocrinology. 2006;147:1895–903.CrossRefPubMed
27.
go back to reference Einarsson S, Ljung A, Brandt Y, Hager M, Madej A. Impact of exogenous ACTH during pro-oestrus on endocrine profile and oestrous cycle characteristics in sows. Reprod Domest Anim. 2007;42:100–4.CrossRefPubMed Einarsson S, Ljung A, Brandt Y, Hager M, Madej A. Impact of exogenous ACTH during pro-oestrus on endocrine profile and oestrous cycle characteristics in sows. Reprod Domest Anim. 2007;42:100–4.CrossRefPubMed
28.
go back to reference Macfarlane MS, Breen KM, Sakurai H, Adams BM, Adams TE. Effect of duration of infusion of stress-like concentrations of cortisol on follicular development and the preovulatory surge of LH in sheep. Anim Reprod Sci. 2000;63:167–75.CrossRefPubMed Macfarlane MS, Breen KM, Sakurai H, Adams BM, Adams TE. Effect of duration of infusion of stress-like concentrations of cortisol on follicular development and the preovulatory surge of LH in sheep. Anim Reprod Sci. 2000;63:167–75.CrossRefPubMed
29.
go back to reference Smith ER, Johnson J, Weick RF, Levine S, Davidson JM. Inhibition of the reproductive system in immature rats by intracerebral implantation of cortisol. Neuroendocrinology. 1971;8:94–106.CrossRefPubMed Smith ER, Johnson J, Weick RF, Levine S, Davidson JM. Inhibition of the reproductive system in immature rats by intracerebral implantation of cortisol. Neuroendocrinology. 1971;8:94–106.CrossRefPubMed
30.
go back to reference Cai L, Sun A, Li H, Tsinkgou A, Yu J, Ying S, Chen Z, Shi Z. Molecular mechanisms of enhancing porcine granulosa cell proliferation and function by treatment in vitro with anti-inhibin alpha subunit antibody. Reprod Biol Endocrinol. 2015;13:26.CrossRefPubMedPubMedCentral Cai L, Sun A, Li H, Tsinkgou A, Yu J, Ying S, Chen Z, Shi Z. Molecular mechanisms of enhancing porcine granulosa cell proliferation and function by treatment in vitro with anti-inhibin alpha subunit antibody. Reprod Biol Endocrinol. 2015;13:26.CrossRefPubMedPubMedCentral
31.
go back to reference Luo WX, Gumen A, Haughian JM, Wiltbank MC. The Role of Luteinizing Hormone in Regulating Gene Expression During Selection of a Dominant Follicle in Cattle. Biol Reprod. 2011;84:369–78.CrossRefPubMed Luo WX, Gumen A, Haughian JM, Wiltbank MC. The Role of Luteinizing Hormone in Regulating Gene Expression During Selection of a Dominant Follicle in Cattle. Biol Reprod. 2011;84:369–78.CrossRefPubMed
32.
go back to reference Nimz M, Spitschak M, Schneider F, Furbass R, Vanselow J. Down-regulation of genes encoding steroidogenic enzymes and hormone receptors in late preovulatory follicles of the cow coincides with an accumulation of intrafollicular steroids. Domest Anim Endocr. 2009;37:45–54.CrossRef Nimz M, Spitschak M, Schneider F, Furbass R, Vanselow J. Down-regulation of genes encoding steroidogenic enzymes and hormone receptors in late preovulatory follicles of the cow coincides with an accumulation of intrafollicular steroids. Domest Anim Endocr. 2009;37:45–54.CrossRef
33.
go back to reference Biran D, Braw-Tal R, Gendelman M, Lavon Y, Roth Z. ACTH administration during formation of preovulatory follicles impairs steroidogenesis and angiogenesis in association with ovulation failure in lactating cows. Domest Anim Endocr. 2015;53:52–9.CrossRef Biran D, Braw-Tal R, Gendelman M, Lavon Y, Roth Z. ACTH administration during formation of preovulatory follicles impairs steroidogenesis and angiogenesis in association with ovulation failure in lactating cows. Domest Anim Endocr. 2015;53:52–9.CrossRef
34.
go back to reference Carreau S, Bourguiba DS, Lambard S, Galeraud-Denis I, Genissel C, Levallet J. Reproductive system: aromatase and estrogens. Mol Cell Endocrino. 2002;193:137–43.CrossRef Carreau S, Bourguiba DS, Lambard S, Galeraud-Denis I, Genissel C, Levallet J. Reproductive system: aromatase and estrogens. Mol Cell Endocrino. 2002;193:137–43.CrossRef
35.
go back to reference Guthrie HD, Bolt DJ, Cooper BS. Changes in Follicular Estradiol-17-Beta, Progesterone and Inhibin Immunoactivity in Healthy and Atretic Follicles during Preovulatory Maturation in the Pig. Domest Anim Endocr. 1993;10:127–40.CrossRef Guthrie HD, Bolt DJ, Cooper BS. Changes in Follicular Estradiol-17-Beta, Progesterone and Inhibin Immunoactivity in Healthy and Atretic Follicles during Preovulatory Maturation in the Pig. Domest Anim Endocr. 1993;10:127–40.CrossRef
36.
go back to reference Guthrie HD, Cooper BS, Welch GR, Zakaria AD, Johnson LA. Atresia in Follicles Grown after Ovulation in the Pig - Measurement of Increased Apoptosis in Granulosa-Cells and Reduced Follicular-Fluid Estradiol-17-Beta. Biol Reprod. 1995;52:920–7.CrossRefPubMed Guthrie HD, Cooper BS, Welch GR, Zakaria AD, Johnson LA. Atresia in Follicles Grown after Ovulation in the Pig - Measurement of Increased Apoptosis in Granulosa-Cells and Reduced Follicular-Fluid Estradiol-17-Beta. Biol Reprod. 1995;52:920–7.CrossRefPubMed
37.
go back to reference Li X, Zhang H, Sheng X, Li B, Zhou J, Xu M, Weng Q, Watanabe G, Taya K. Immunoreactivities of androgen receptor, estrogen receptors, p450arom, p450c17 proteins in wild ground squirrels ovaries during the nonbreeding and breeding seasons. J Ovarian Res. 2012;5:26.CrossRefPubMedPubMedCentral Li X, Zhang H, Sheng X, Li B, Zhou J, Xu M, Weng Q, Watanabe G, Taya K. Immunoreactivities of androgen receptor, estrogen receptors, p450arom, p450c17 proteins in wild ground squirrels ovaries during the nonbreeding and breeding seasons. J Ovarian Res. 2012;5:26.CrossRefPubMedPubMedCentral
38.
go back to reference Hsueh AJ, Adashi EY, Jones PB, Welsh Jr TH. Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr Rev. 1984;5:76–127.CrossRefPubMed Hsueh AJ, Adashi EY, Jones PB, Welsh Jr TH. Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr Rev. 1984;5:76–127.CrossRefPubMed
39.
go back to reference Garverick HA, Polge C, Flint AP. Oestradiol administration raises luteal LH receptor levels in intact and hysterectomized pigs. J Reprod Fertil. 1982;66:371–7.CrossRefPubMed Garverick HA, Polge C, Flint AP. Oestradiol administration raises luteal LH receptor levels in intact and hysterectomized pigs. J Reprod Fertil. 1982;66:371–7.CrossRefPubMed
41.
go back to reference Themmen APN, Huhtaniemi IT. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr Rev. 2000;21:551–83.CrossRefPubMed Themmen APN, Huhtaniemi IT. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr Rev. 2000;21:551–83.CrossRefPubMed
42.
go back to reference Sapolsky RM. How Do Glucocorticoids Influence Stress Responses? Integrating Permissive, Suppressive, Stimulatory, and Preparative Actions. Endocr Rev. 2000;21:55–89.PubMed Sapolsky RM. How Do Glucocorticoids Influence Stress Responses? Integrating Permissive, Suppressive, Stimulatory, and Preparative Actions. Endocr Rev. 2000;21:55–89.PubMed
43.
go back to reference Yung Y, Aviel-Ronen S, Maman E, Rubinstein N, Avivi C, Orvieto R, Hourvitz A. Localization of luteinizing hormone receptor protein in the human ovary. Mol Hum Reprod. 2014;20:844–9.CrossRefPubMed Yung Y, Aviel-Ronen S, Maman E, Rubinstein N, Avivi C, Orvieto R, Hourvitz A. Localization of luteinizing hormone receptor protein in the human ovary. Mol Hum Reprod. 2014;20:844–9.CrossRefPubMed
Metadata
Title
ACTH-induced stress in weaned sows impairs LH receptor expression and steroidogenesis capacity in the ovary
Authors
H. S. Zhu
Z. Qian
H. L. Liu
E. D. Bao
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2016
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-016-0214-5

Other articles of this Issue 1/2016

Reproductive Biology and Endocrinology 1/2016 Go to the issue