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RESEARCH ARTICLE

Involvement of prolactin in the meloxicam-dependent inflammatory response of the gonadotropic axis to prolonged lipopolysaccharide treatment in anoestrous ewes

Andrzej P. Herman A C , Agata Krawczyńska A , Joanna Bochenek A , Hanna Antushevich A , Anna Herman B and Dorota Tomaszewska-Zaremba A
+ Author Affiliations
- Author Affiliations

A Polish Academy of Sciences, The Kielanowski Institute of Animal Physiology and Nutrition, 05-110 Jabłonna, Poland.

B The Academy of Cosmetics and Health Care, 13 Podwale Street, 00-252 Warsaw, Poland.

C Corresponding author. Email: andrewherman@wp.pl

Reproduction, Fertility and Development 28(7) 914-923 https://doi.org/10.1071/RD13435
Submitted: 21 December 2013  Accepted: 20 October 2014   Published: 28 November 2014

Abstract

An immune challenge can affect the reproductive process in females. Peripheral administration of bacterial endotoxin (lipopolysaccharide; LPS) decreases LH secretion and disrupts ovarian cyclicity. The aim of the present study was to determine the effects of a cyclo-oxygenase (COX)-2 inhibitor (meloxicam) on gonadotropin-releasing hormone (GnRH) and LH secretion in anoestrous ewes during systemic inflammation induced by LPS. LPS (400 ng kg–1 per day) suppressed LH release. In three individuals, meloxicam (500 μg kg–1, i.v.) abolished LPS-induced LH suppression. In another three ewes LH was ineffective. Similar changes were observed in hypothalamic GnRH expression. The effect of meloxicam depended on the circulating level of prolactin: meloxicam abolished inflammatory-dependent suppression of GnRH and LH secretion when plasma prolactin levels were similar to those in untreated animals, but was ineffective in those with elevated levels of prolactin. We conclude that COX-2 inhibitors minimise the negative effect of inflammation on the reproductive system but that this effect may be antagonised by prolactin.

Additional keywords: gonadotrophin-releasing hormone, hypothalamus, LH.


References

Anderson, G. D., Hauser, S. D., McGarity, K. L., Bremer, M. E., Isakson, P. C., and Gregory, S. A. (1996). Selective inhibition of cyclooxygenase (COX)-2 reverses inflammation and expression of COX-2 and interleukin 6 in rat adjuvant arthritis. J. Clin. Invest. 97, 2672–2679.
Selective inhibition of cyclooxygenase (COX)-2 reverses inflammation and expression of COX-2 and interleukin 6 in rat adjuvant arthritis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjsFKjsbg%3D&md5=811cd943656108a69136b3a4256313acCAS | 8647962PubMed |

Battaglia, D. F., Brown, M. E., Krasa, H. B., Thrun, L. A., Viguié, C., and Karsch, F. J. (1998). Systemic challenge with endotoxin stimulates corticotropin-releasing hormone and arginine vasopressin secretion into hypophyseal portal blood: coincidence with gonadotropin-releasing hormone suppression. Endocrinology 139, 4175–4181.
| 1:CAS:528:DyaK1cXmsVGnu7w%3D&md5=d8b03961b2db112c57804506c6854757CAS | 9751497PubMed |

Battaglia, D. F., Beaver, A. B., Harris, T. G., Tanhehco, E., Viguié, C., and Karsch, F. J. (1999). Endotoxin disrupts the estradiol-induced luteinizing hormone surge: interference with estradiol signal reading, not surge release. Endocrinology 140, 2471–2479.
| 1:CAS:528:DyaK1MXjtlKhtrw%3D&md5=7b3eb6082191c69260908b785108ff29CAS | 10342831PubMed |

Battaglia, D. F., Krasa, H. B., Padmananbhan, V., Viguie, C., and Karsch, F. J. (2000). Endocrine alterations that underlie endotoxininduced disruption of the follicular phase in ewes. Biol. Reprod. 62, 45–53.
Endocrine alterations that underlie endotoxininduced disruption of the follicular phase in ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhslKlsg%3D%3D&md5=77921c52dac06ef0103f38397f476a4bCAS | 10611066PubMed |

Bondanelli, M., Zatelli, M. C., Ambrosio, M. R., and degli Uberti, E. C. (2008). Systemic illness. Pituitary 11, 187–207.
Systemic illness.Crossref | GoogleScholarGoogle Scholar | 18404385PubMed |

Bradford, M. M. (1976). Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.
Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=74dc2e9d3f64a3c2f7f031b32f8d18fbCAS | 942051PubMed |

Breen, K. M., Billings, H. J., Debus, N., and Karsch, F. J. (2004). Endotoxin inhibits the surge secretion of gonadotropin-releasing hormone via a prostaglandin-independent pathway. Endocrinology 145, 221–227.
Endotoxin inhibits the surge secretion of gonadotropin-releasing hormone via a prostaglandin-independent pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVWgt7bN&md5=1a3f386ac0e77ce38e6e42f2915ccca6CAS | 14551234PubMed |

Caldani, M., Batailler, M., Thiery, J. C., and Dubois, M. P. (1988). LHRH immunoreactive structures in the sheep brain. Histochemistry 89, 129–139.
LHRH immunoreactive structures in the sheep brain.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3osFWlsw%3D%3D&md5=d70ca3aef39ea567ef3eadea164d8966CAS | 3294216PubMed |

Cheung, C. Y. (1983). Prolactin suppresses luteinizing hormone secretion and pituitary responsiveness to luteinizing hormone-releasing hormone by a direct action at the anterior pituitary. Endocrinology 113, 632–638.
Prolactin suppresses luteinizing hormone secretion and pituitary responsiveness to luteinizing hormone-releasing hormone by a direct action at the anterior pituitary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXkvVartr0%3D&md5=248218317be6e2ebc908edb1f97a08c7CAS | 6347662PubMed |

Coleman, E. S., Elsasser, T. H., Kemppainen, R. J., Coleman, D. A., and Sartin, J. L. (1993). Effect of endotoxin on pituitary hormone secretion in sheep. Neuroendocrinology 58, 111–122.
Effect of endotoxin on pituitary hormone secretion in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1Cnt7w%3D&md5=1a1764c2c03bc0a040ea071c8b420f0eCAS | 8264844PubMed |

Cruz, R., Quintana-Hau, J. D., González, J. R., Tornero-Montaño, R., Baiza-Durán, L. M., and Vega, L. (2008). Effects of an ophthalmic formulation of meloxicam on COX-2 expression, PGE2 release, and cytokine expression in a model of acute ocular inflammation. Br. J. Ophthalmol. 92, 120–125.
Effects of an ophthalmic formulation of meloxicam on COX-2 expression, PGE2 release, and cytokine expression in a model of acute ocular inflammation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2sjmtFSktQ%3D%3D&md5=2ee623b32f73b08ba19325e6b8416879CAS | 17962388PubMed |

Daniel, J. A., Abrams, M. S., de Souza, L., Wagner, C. G., Whitlock, B. K., and Sartin, J. L. (2003). Endotoxin inhibition of luteinizing hormone in sheep. Domest. Anim. Endocrinol. 25, 13–19.
Endotoxin inhibition of luteinizing hormone in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVCiu7w%3D&md5=8514d5c1ceef1331035f1e7385fbe5d9CAS | 12963096PubMed |

Debus, N., Breen, K. M., Barrell, G. K., Billings, H. J., Brown, M., Young, E. A., and Karsch, F. J. (2002). Does cortisol mediate endotoxin-induced inhibition of pulsatile luteinizing hormone and gonadotropin-releasing hormone secretion? Endocrinology 143, 3748–3758.
Does cortisol mediate endotoxin-induced inhibition of pulsatile luteinizing hormone and gonadotropin-releasing hormone secretion?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xnt1ygs7k%3D&md5=0fd834fd99264de05eba9ee583d1d476CAS | 12239084PubMed |

Fox, S. R., Hoefer, M. T., Bartke, A., and Smith, M. S. (1987). Suppression of pulsatile LH secretion, pituitary GnRH receptor content and pituitary responsiveness to GnRH by hyperprolactinemia in the male rat. Neuroendocrinology 46, 350–359.
Suppression of pulsatile LH secretion, pituitary GnRH receptor content and pituitary responsiveness to GnRH by hyperprolactinemia in the male rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXltV2kt7k%3D&md5=771eaf83e566079a66cb0ce14ef93ccfCAS | 2823160PubMed |

Gadient, R. A., and Otten, U. (1993). Differential expression of interleukin-6 (IL-6) and interleukin-6 receptor (IL-6R) mRNA in rat hypothalamus. Neurosci. Lett. 153, 13–16.
Differential expression of interleukin-6 (IL-6) and interleukin-6 receptor (IL-6R) mRNA in rat hypothalamus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVKqtrY%3D&md5=a3b48acf33b6982b3b232401095f4f32CAS | 8510817PubMed |

Grattan, D. R., Jasoni, C. L., Liu, X., Anderson, G. M., and Herbison, A. E. (2007). Prolactin regulation of gonadotropin-releasing hormone neurons to suppress luteinizing hormone secretion in mice. Endocrinology 148, 4344–4351.
Prolactin regulation of gonadotropin-releasing hormone neurons to suppress luteinizing hormone secretion in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslCntbY%3D&md5=4b3af78d07b34d03721838aad274d485CAS | 17569755PubMed |

Harris, T. G., Battaglia, D. F., Brown, M. E., Brown, M. B., Carlson, N. E., Viguié, C., Williams, C. Y., and Karsch, F. J. (2000). Prostaglandins mediate the endotoxin-induced suppression of pulsatile gonadotropin-releasing hormone and luteinizing hormone secretion in the ewe. Endocrinology 141, 1050–1058.
| 1:CAS:528:DC%2BD3cXisFOrsbs%3D&md5=9472d7bcafc80e157c89ec8150a66d63CAS | 10698181PubMed |

Haziak, K., Herman, A. P., and Tomaszewska-Zaremba, D. (2013). Effect of LPS on the LH release and gene expression of LH-β, GnRH-R and TLR4 in the anterior pituitary of follicular phase ewes: in vitro study. J. Anim. Feed Sci. 22, 97–105.

Herman, A. P., and Tomaszewska-Zaremba, D. (2010). Effect of endotoxin on the expression of GnRH and GnRHR genes in the hypothalamus and anterior pituitary gland of anestrous ewes. Anim. Reprod. Sci. 120, 105–111.
Effect of endotoxin on the expression of GnRH and GnRHR genes in the hypothalamus and anterior pituitary gland of anestrous ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFWrsbY%3D&md5=36f595ec5990c57d23d3da3101100f72CAS | 20427135PubMed |

Herman, A. P., Romanowicz, K., and Tomaszewska-Zaremba, D. (2010). Effect of LPS on reproductive system at the level of the pituitary of anestrous ewes. Reprod. Domest. Anim. 45, e351–e359.
Effect of LPS on reproductive system at the level of the pituitary of anestrous ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WrsLbI&md5=19e0eeb5d0af77df6418acc53bc67b63CAS | 20345594PubMed |

Herman, A. P., Misztal, T., Romanowicz, K., and Tomaszewska-Zaremba, D. (2012). Central injection of exogenous IL-1β in the control activities of hypothalamic–pituitary–gonadal axis in anestrous awes. Reprod. Domest. Anim. 47, 44–52.
Central injection of exogenous IL-1β in the control activities of hypothalamic–pituitary–gonadal axis in anestrous awes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XislWmtrs%3D&md5=3d29d7cb4427827ce80fc76caedf8f81CAS | 21595758PubMed |

Huntjens, D. R., Danhof, M., and Della Pasqua, O. E. (2005). Pharmacokinetic–pharmacodynamic correlations and biomarkers in the development of COX-2 inhibitors. Rheumatology 44, 846–859.
Pharmacokinetic–pharmacodynamic correlations and biomarkers in the development of COX-2 inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslyrsb4%3D&md5=685d4f93c62aed144ae31bddda0b06cfCAS | 15855183PubMed |

Huntjens, D. R., Spalding, D. J., Danhof, M., and Della Pasqua, O. E. (2006). Correlation between in vitro and in vivo concentration–effect relationships of naproxen in rats and healthy volunteers. Br. J. Pharmacol. 148, 396–404.
Correlation between in vitro and in vivo concentration–effect relationships of naproxen in rats and healthy volunteers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsV2ku7w%3D&md5=753643abdbf272e9f664c01ffa6c712dCAS | 16682968PubMed |

Igaz, P., Salvi, R., Rey, J. P., Glauser, M., Pralong, F. P., and Gaillard, R. C. (2006). Effects of cytokines on gonadotropin-releasing hormone (GnRH) gene expression in primary hypothalamic neurons and in GnRH neurons immortalized conditionally. Endocrinology 147, 1037–1043.
Effects of cytokines on gonadotropin-releasing hormone (GnRH) gene expression in primary hypothalamic neurons and in GnRH neurons immortalized conditionally.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVeiug%3D%3D&md5=994fd7fbe5487f968c1fc6a852b08497CAS | 16282355PubMed |

Kalra, P. S., Edwards, T. G., Xu, B., Jain, M., and Kalra, S. P. (1998). The anti-gonadotropic effects of cytokines: the role of neuropeptides. Domest. Anim. Endocrinol. 15, 321–332.
The anti-gonadotropic effects of cytokines: the role of neuropeptides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvVKjtrw%3D&md5=3a313a5bad61f32caebd2410f4b74817CAS | 9785036PubMed |

Kang, S. S., Kim, S. R., Leonhardt, S., Jarry, H., Wuttke, W., and Kim, K. (2000). Effect of interleukin-1β on gonadotropin-releasing hormone (GnRH) and GnRH receptor gene expression in castrated male rats. J. Neuroendocrinol. 12, 421–429.
Effect of interleukin-1β on gonadotropin-releasing hormone (GnRH) and GnRH receptor gene expression in castrated male rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsVKjtbo%3D&md5=792ec925d39c269c5558f438bcf24409CAS | 10792581PubMed |

Karsch, F. J., Battaglia, D. F., Breen, K. M., Debus, N., and Harris, T. G. (2002). Mechanisms for ovarian cycle disruption by immune/inflammatory stress. Stress 5, 101–112.
Mechanisms for ovarian cycle disruption by immune/inflammatory stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvFChs7k%3D&md5=5028ce170dce59854fd757b86fc3b7bbCAS | 12186688PubMed |

Kochman, H., and Kochman, K. (1977). Purifcation of ovine and bovine prolactins on DEAE cellulose chromatography and preparative polyacrylamide gel electrophoresis. Bull. Acad Pol. Sci. Ser. Sci. Biol. 25, 67–70.
| 1:CAS:528:DyaE2sXhvVCkurY%3D&md5=24d16f27f3b116aad503f586d0858153CAS |

Kokot, F., and Stupnicki, R. (1985). ‘Metody Radioimmunologiczne i Radiokompetyncyjne Stosowane w Klinice.’ 2nd edn. (Państwowe Zakłady Wydawnictw Lekarskich: Warsaw.)

Koressaar, T., and Remm, M. (2007). Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289–1291.
Enhancements and modifications of primer design program Primer3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVOjur0%3D&md5=075fbb8e6d32ba845be874252a0983c5CAS | 17379693PubMed |

L’Hermite, M., Niswender, G. D., Reichert, L. E., and Midgley, A. R. (1972). Serum follicle stimulating hormone in sheep as measured by radioimmunoassay. Biol. Reprod. 6, 325–332.
| 1:CAS:528:DyaE38XksVGqt74%3D&md5=3f3d22b49906fe7a39e1cfa4567450e9CAS | 5062832PubMed |

Martínez, R. V., Reval, M., Campos, M. D., Terron, J. A., Dominguez, R., and Lopez-Munoz, F. J. (2002). Involvement of peripheral cyclooxygenase-1 andbcyclooxygenase-2 in inflammatory pain. J. Pharm. Pharmacol. 54, 405–412.
Involvement of peripheral cyclooxygenase-1 andbcyclooxygenase-2 in inflammatory pain.Crossref | GoogleScholarGoogle Scholar | 11902807PubMed |

McMahan, C. J., Slack, J. L., Mosley, B., Cosman, D., Lupton, S. D., Brunton, L. L., Grubin, C. E., Wignall, J. M., Jenkins, N. A., and Brannan, C. I. (1991). A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J. 10, 2821–2832.
| 1:CAS:528:DyaK38Xls12iu78%3D&md5=7e64b6d1764ba1a27742f1a70f62bc18CAS | 1833184PubMed |

Milenković, L., D’Angelo, G., Kelly, P. A., and Weiner, R. I. (1994). Inhibition of gonadotropin hormone-releasing hormone release by prolactin from GT1 neuronal cell lines through prolactin receptors. Proc. Natl Acad. Sci. USA 91, 1244–1247.
Inhibition of gonadotropin hormone-releasing hormone release by prolactin from GT1 neuronal cell lines through prolactin receptors.Crossref | GoogleScholarGoogle Scholar | 8108395PubMed |

Netea, M. G., Kullberg, B. J., and Van der Meer, J. W. M. (2000). Circulating cytokines as mediators of fever. Clin. Infect. Dis. 31, S178–S184.
Circulating cytokines as mediators of fever.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXos1yrt7g%3D&md5=2e74584fc0917fb0da34ed71700b80b2CAS | 11113021PubMed |

Oakley, A. E., Breen, K. M., Clarke, I. J., Karsch, F. J., Wagenmaker, E. R., and Tilbrook, A. J. (2009a). Cortisol reduces gonadotropin-releasing hormone pulse frequency in follicular phase ewes: influence of ovarian steroids. Endocrinology 150, 341–349.
Cortisol reduces gonadotropin-releasing hormone pulse frequency in follicular phase ewes: influence of ovarian steroids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmt1aqsQ%3D%3D&md5=51feb5609bb5b4905f34658db414d6e4CAS | 18801903PubMed |

Oakley, A. E., Breen, K. M., Tilbrook, A. J., Wagenmaker, E. R., and Karsch, F. J. (2009b). Role of estradiol in cortisol-induced reduction of luteinizing hormone pulse frequency. Endocrinology 150, 2775–2782.
Role of estradiol in cortisol-induced reduction of luteinizing hormone pulse frequency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVCqurk%3D&md5=87370793d504d7172f56db88636476b5CAS | 19179435PubMed |

Peter, A. T., Bosu, W. T. K., and De Decher, R. J. (1989). Suppression of preovulatory luteinizing hormone surges in heifers after intrauterine infusions of Escherichia coli endotoxin. Am. J. Vet. Res. 50, 368–373.
| 1:CAS:528:DyaL1MXhsV2mtLw%3D&md5=e271e9a71173a5a863ae5b7a8b170922CAS | 2648904PubMed |

Pfaffl, M. W., Tichopad, A., Prgomet, C., and Neuvians, T. P. (2004). Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnol. Lett. 26, 509–515.
Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvF2mtLk%3D&md5=6a2360a699196d152c2821ed6b31ca25CAS | 15127793PubMed |

Rasmussen, R. (2001). Quantification on the LightCycler. In ‘Rapid Cycle Real-Time PCR Methods and Applications’. (Eds S. Meuer, C. Wittwer and K. Nakagawara K.) pp. 21–34. (Springer Press: Berlin.)

Rivest, S., and Rivier, C. (1993). Centrally injected interleukin-1 beta inhibits hypothalamic LHRH secretion and circulating LH levels via prostaglandins in rats. J. Neuroendocrinol. 5, 445–450.
Centrally injected interleukin-1 beta inhibits hypothalamic LHRH secretion and circulating LH levels via prostaglandins in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVegsbc%3D&md5=3edef2d8cce230221f32269e8a225852CAS | 8401568PubMed |

Rivier, C., and Vale, W. (1990). Cytokines act within the brain to inhibit luteinizing hormone secretion and ovulation in the rat. Endocrinology 127, 849–856.
Cytokines act within the brain to inhibit luteinizing hormone secretion and ovulation in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXltFemtLo%3D&md5=ae0c1b02c15928b087ac60efded748afCAS | 2115435PubMed |

Scotland, P. E., Patil, M., Belugin, S., Henry, M. A., Goffin, V., Hargreaves, K. M., and Akopian, A. N. (2011). Endogenous prolactin generated during peripheral inflammation contributes to thermal hyperalgesia. Eur. J. Neurosci. 34, 745–754.
Endogenous prolactin generated during peripheral inflammation contributes to thermal hyperalgesia.Crossref | GoogleScholarGoogle Scholar | 21777304PubMed |

Smith, M. S. (1978). A comparison of pituitary responsiveness to luteinizing hormone-releasing hormone during lactation and the estrous cycle of the rat. Endocrinology 102, 114–120.
A comparison of pituitary responsiveness to luteinizing hormone-releasing hormone during lactation and the estrous cycle of the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXpvFGltg%3D%3D&md5=5fe43e3a2df301ca461e6687402cb103CAS | 369817PubMed |

Smith, M. S. (1982). Effect of pulsatile gonadotrophin-releasing hormone on the release of luteinizing hormone and follicle-stimulating hormone in vitro by anterior pituitaries from lactating and cycling rats. Endocrinology 110, 882–891.
Effect of pulsatile gonadotrophin-releasing hormone on the release of luteinizing hormone and follicle-stimulating hormone in vitro by anterior pituitaries from lactating and cycling rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhsFGqsbs%3D&md5=cab3fdfd6e4dfa7c63216c9ce27cfa29CAS |

Sortino, M. A., and Wise, P. M. (1989). Effect of hyperprolactinemia on luteinizing hormone and prolactin secretion assessed using the reverse hemolytic plaque assay. Biol. Reprod. 41, 618–625.
Effect of hyperprolactinemia on luteinizing hormone and prolactin secretion assessed using the reverse hemolytic plaque assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkvFSgtw%3D%3D&md5=7896a9a42409977618a6c3159311c822CAS | 2695175PubMed |

Stupnicki, R., and Madej, A. (1976). Radioimmunoassay of LH in blood plasma of farm animals. Endokrinologie 68, 6–13.
| 1:CAS:528:DyaE2sXislClug%3D%3D&md5=0fcfc4396e42dbf565fae9f1739edb8fCAS | 1001269PubMed |

Tilders, F. J. H., DeRijk, R. H., Van Dam, A., Vincent, V. A. M., Schotanus, K., and Persoons, J. H. A. (1994). Activation of the hypothalamus–pituitary–adrenal axis by bacterial endotoxins: routes and intermediate signals. Psychoneuroendocrinology 19, 209–232.
Activation of the hypothalamus–pituitary–adrenal axis by bacterial endotoxins: routes and intermediate signals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFKisLs%3D&md5=cc8c9b043b4addf12db8e146dd38ed8aCAS |

Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., and Rozen, S. G. (2012). Primer3 – new capabilities and interfaces. Nucleic Acids Res. 40, e115.
Primer3 – new capabilities and interfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Kjs7nF&md5=5ec22ab3361b1043c85c9fd52f412604CAS | 22730293PubMed |

Vane, J. R., and Botting, R. M. (2001). Formation and actions of prostaglandins and inhibition of their synthesis. In ‘Therapeutic roles of selective COX-2 inhibitors’. (Eds J. R. Vane and R. M. Botting.) pp. 1–47. (William Harvey Press: London.)

Vitkovic, L., Bockaert, J., and Jacque, C. (2000). ‘Inflammatory’ cytokines: neuromodulators in normal brain? J. Neurochem. 74, 457–471.
‘Inflammatory’ cytokines: neuromodulators in normal brain?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFOrsA%3D%3D&md5=4599b7de99cf956fd43b6e54b48d2c77CAS | 10646496PubMed |

Walsh, R. J., Slaby, F. J., and Posner, B. I. (1987). A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 120, 1846–1850.
A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXitVyjtrY%3D&md5=3dd725fe90b46f6af56c21a859536c5dCAS | 3569115PubMed |

Walsh, R. J., Mangurian, L. P., and Posner, B. I. (1990). Prolactin receptors in the primate choroid plexus. J. Anat. 168, 137–141.
| 1:CAS:528:DyaK3cXksFaksLc%3D&md5=8726b083f4a7236b5336639b386200a2CAS | 2323989PubMed |

Welento, J., Szteyn, S., and Milartz, Z. (1969). Observations on the stereotaxic configuration of the hypothalamus nuclei in the sheep. Anat. Anz. 124, 1.
| 1:STN:280:DyaF1M3gs1Oisw%3D%3D&md5=fbd21e9a537f5aeff6cf405c0661a653CAS | 4891518PubMed |

Williams, E. J., Fischer, D. P., Noakes, D. E., England, G. E., Rycroft, A., Dobson, H., and Sheldon, I. M. (2007). The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology 68, 549–559.
The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlWqu7w%3D&md5=f0d0e76a0e8301403650a8a89fb39d7fCAS | 17574659PubMed |

Williams, E. J., Sibley, K., Miller, A. N., Lane, E. A., Fishwick, J., Nash, D. M., Herath, S., England, G. C., Dobson, H., and Sheldon, I. M. (2008). The effect of Escherichia coli lipopolysaccharide and tumour necrosis factor alpha on ovarian function. Am. J. Reprod. Immunol. 60, 462–473.
The effect of Escherichia coli lipopolysaccharide and tumour necrosis factor alpha on ovarian function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGgt7fK&md5=d3269eca38d3407e40dc2bc5cd46069bCAS | 19238751PubMed |

Wolińska, E., Polkowska, J., and Domański, E. (1977). The hypothalamic centers involved in the control of production and release of prolactin in sheep. J. Endocrinol. 73, 21–29.
The hypothalamic centers involved in the control of production and release of prolactin in sheep.Crossref | GoogleScholarGoogle Scholar | 323394PubMed |

Yoo, M. J., Nishihara, M., and Takahashi, M. (1997). Involvement of prostaglandins in suppression of gonadotropin-releasing hormone pulse generator activity by tumor necrosis factor-α. J. Reprod. Dev. 43, 181–187.
Involvement of prostaglandins in suppression of gonadotropin-releasing hormone pulse generator activity by tumor necrosis factor-α.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltlWkurc%3D&md5=ab96c4e6bb38539e29712a229b7172edCAS |