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Prolactin receptor regulates the seasonal reproduction of striped hamsters

Published online by Cambridge University Press:  22 June 2021

Huiliang Xue ,
Jinhui Xu ,
Ming Wu ,
Lei Chen  and
Laixiang Xu Open the ORCID record for Laixiang Xu [Opens in a new window]
Huiliang Xue
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong Province 273165, China
Jinhui Xu
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong Province 273165, China
Ming Wu
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong Province 273165, China
Lei Chen
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong Province 273165, China
Laixiang Xu*
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong Province 273165, China
*
Author for correspondence: Laixiang Xu. College of Life Sciences, Qufu Normal University, No. 57 Jingxuan West Road, Qufu, Shandong Province 273165, China. Tel: +86 0537 4458169. Email: [email protected]
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Summary

In this study, differential mRNA expression patterns of prolactin receptor (PRLR) in the hypothalamus and gonads, and the correlation with follicle stimulating hormone (FSH) and luteinizing hormone (LH) in striped hamster serum from spring, summer, autumn and winter were analyzed. Mature female and male striped hamsters in oestrus were used. Expression levels of PRLR in the hypothalamus, ovaries and testis from the summer and winter individuals were significantly higher compared with levels from the spring and autumn, whereas FSH and LH serum concentrations from summer and winter individuals were significantly lower compared with that from the spring and autumn. PRLR expression levels in hypothalamus, ovaries and testis were negatively correlated with FSH and LH serum concentrations, illustrating that PRLR might negatively regulate seasonal reproductive activity. PRLR expression levels in ovaries and testes were significantly higher compared with levels in the hypothalamus, suggesting that the regulative effects of PRLR in gonads might be significantly higher compared with that in the hypothalamus. Furthermore, PRLR expression levels from the spring, summer, autumn and winter seasons in the hypothalamus and gonads were significantly higher in females compared with levels in males, indicating that the regulative effect of PRLR might be sex dependent. Taken together, this study helps to understand in depth the seasonal regulative reproduction mechanism of striped hamsters to reasonably control population abundance.

Keywords

PRLRSeasonal reproductionSexStriped Hamsters
Type
Research Article
Information
Zygote , Volume 30 , Issue 1 , February 2022 , pp. 40 - 47
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Asad, AS, Nicola Candia, AJ, Gonzalez, N, Zuccato, CF, Abt, A, Orrillo, SJ, Lastra, Y, De Simone, E, Boutillon, F, Goffin, V, Seilicovich, A, Pisera, DA, Ferraris, MJ and Candolfi, M (2019). Prolactin and its receptor as therapeutic targets in glioblastoma multiforme. Sci Rep 9, 19578.CrossRefGoogle ScholarPubMed
Badura, LL and Goldman, BD (1997). Anterior pituitary release of prolactin is inhibited by exposure to short photoperiod. J Neuroendocrinol 9, 341–5.10.1046/j.1365-2826.1997.00585.xCrossRefGoogle ScholarPubMed
Bole-Feysot, C, Goffin, V, Edery, M, Binart, N and Kelly, PA (1998). Prolactin (PRL) and its receptor actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19, 225–68.CrossRefGoogle ScholarPubMed
Bolyakov, A and Paduch, DA (2011). Prolactin in men’s health and disease. Curr Opin Urol 21, 527–34.CrossRefGoogle ScholarPubMed
Boulay, JL and Paul, WE (1992). The interleukin-4-related lymphokines and their binding to hematopoietin receptors. J Biol Chem 267, 20525–8.CrossRefGoogle ScholarPubMed
Bubenik, GA, Morris, JM, Schams, D and Claus, A (1982). Photoperiodicity and circannual levels of LH, FSH and testosterone in normal and castrated male, white-tailed deer. J Biol Chem 60, 788–93.Google ScholarPubMed
Calogero, AE, Weber, RF and D’Agata, R (1993). Effects of rat prolactin on gonadotropin-releasing hormone secretion by the explanted male rat hypothalamus. Neuroendocrinology 57, 152–8.CrossRefGoogle ScholarPubMed
Chiu, S, Koos, RD and Wise, PM (1992). Detection of prolactin receptor (PRL-R) mRNA in the rat hypothalamus and pituitary gland. Endocrinology 130, 1747–9.Google ScholarPubMed
Ciereszko, R, Opałka, M, Kamińska, B, Kamiński, T and Dusza, L (2002). Prolactin involvement in the regulation of the hypothalamic–pituitary–ovarian axis during the early luteal phase of the porcine estrous cycle. Anim Reprod Sci 69, 99–115.CrossRefGoogle ScholarPubMed
Clarke, LA, Wathes, DC and Jabbour, HN (1997). Expression and localization of prolactin receptor messenger ribonucleic acid in red deer ovary during the estrous cycle and pregnancy. Biol Reprod 57, 865–72.CrossRefGoogle Scholar
Clayton, RN and Bailey, LC (1982). Hyperprolactinemia attenuates the gonadotrophin releasing hormone receptor response to gonadectomy in rats. J Endocrinol 95, 267–74.CrossRefGoogle ScholarPubMed
Clevenger, CV, Gadd, SL and Zheng, JM (2009). New mechanism for PRLr action in breast cancer. Trends Endocrinol Metab 20, 223–9.CrossRefGoogle ScholarPubMed
Curlewis, JD (1992). Seasonal prolactin secretion and its role in seasonal reproduction: a review. Reprod Fertil Dev 4, 1–23.CrossRefGoogle ScholarPubMed
Exbrayat, JM and Morel, G (2003). Visualization of gene expression of prolactin-receptor (PRL-R) by in situ hybridization in reproductive organs of Typhlonectes compressicauda, a gymnophionan amphibian. Cell Tissue Res 312, 361–7.CrossRefGoogle ScholarPubMed
Gregory, SJ, Brooks, J, McNeilly, AS, Ingleton, PM and Tortonese, DJ (2000). Gonadotroph-lactotroph associations and expression of prolactin receptors in the equine pituitary gland throughout the seasonal reproductive cycle. J Reprod Fertil 119, 223–31.CrossRefGoogle ScholarPubMed
Harris, JM, Irvine, CHG and Evans, MJ (1983). Seasonal changes in serum levels of FSH, LH and testosterone and in semen parameters in stallions. Theriogenology 19, 311–22.CrossRefGoogle Scholar
Horseman, ND and Yu-Lee, LY (1994). Transcriptional regulation by the helix bundle peptide hormones: growth hormone, prolactin, and hematopoietic cytokines. Endocr Rev 15, 627–49.CrossRefGoogle ScholarPubMed
Koike, K, Kadowaki, K, Hirota, K, Ohmichi, M, Ikegami, H, Sawada, T, Miyake, A and Tanizawa, O (1993). Prolactin stimulates [3H]dopamine release from dispersed rat tubero-infundibular dopaminergic neurons and dopamine decreases gonadotropin-releasing hormone release induced by calcium ionophore. Acta Endocrinol (Copenh) 129, 548–53.CrossRefGoogle ScholarPubMed
Kugu, K, Taketani, Y and Mizuno, M (1989). Stimulatory action of prolactin on gonadotropin secretion in vitro . Endocrinol Jpn 36, 509–14.CrossRefGoogle ScholarPubMed
Lincoln, GA and Short, RV (1980). Seasonal breeding: nature’s contraceptive. Recent Prog Horm Res 36, 1–52.Google ScholarPubMed
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25, 402–8.CrossRefGoogle Scholar
Luo, ZX, Chen, W and Gao, W (2000). Chinese Fauna·Beast Gang, vol. VI. Beijing: Science Press, pp. 28–38.Google Scholar
Milenković, L, D’Angelo, G, Kelly, PA and Weiner, RI (1994). Inhibition of gonadotropin hormone-releasing hormone release by prolactin from GT1 neuronal cell lines through prolactin receptors. Proc Natl Acad Sci USA 91, 1244–7.CrossRefGoogle ScholarPubMed
Mu, CW, Wang, YY and Ren, WX (1999). Studies on the biological characteristics and prevention and treatment for the striped hamster. Gansu Agric Sci Technol 1, 39.Google Scholar
Muduuli, DS, Sanford, LM, Palmer, WM and Howland, BE (1979). Secretory patterns and circadian and seasonal changes in luteinizing hormone, follicle stimulating hormone, prolactin and testosterone in the male pygmy goat. J Anim Sci 49, 543–53.CrossRefGoogle ScholarPubMed
Mustafa, A, Nyberg, F, Bogdanovic, N, Islam, A, Suliman, I, Lindgren, U, Roos, P and Adem, A (1995). Prolactin binding sites in rat brain and liver: effects of long-term ovariectomy and ovarian steroids. Neurosci Lett 200, 179–82.CrossRefGoogle ScholarPubMed
Niall, HD, Hogan, ML, Sauer, R, Rosenblum, IY and Greenwood, FC (1971). Sequences of pituitary and placental lactogenic and growth hormones: evolution from a primordial peptide by gene reduplication. Proc Natl Acad Sci USA 68, 866–70.CrossRefGoogle ScholarPubMed
Ohkubo, T, Tanaka, M, Nakashima, K and Sharp, PJ (1998). Relationship between prolactin receptor mRNA in the anterior pituitary gland and hypothalamus and reproductive state in male and female bantams (Gallus domesticus). Gen Comp Endocrinol 111, 167–76.CrossRefGoogle Scholar
Sarkar, DK and Yen, SS (1985). Hyperprolactinemia decreases the luteinizing hormone-releasing hormone concentration in pituitary portal plasma: a possible role for beta-endorphin as a mediator. Endocrinology 116, 2080–4.CrossRefGoogle ScholarPubMed
Shamgochian, MD, Avakian, C, Truong, NH, Stone, S, Tang, KT and Devito, WJ (1995). Regulation of prolactin receptor expression by estradiol in the female rat brain. Neuroreport 6, 2537–41.CrossRefGoogle ScholarPubMed
Shi, ZD, Huang, YM, Liu, Z, Liu, Y, Li, XW, Proudman, JA and Yu, RC (2007). Seasonal and photoperiodic regulation of secretion of hormones associated with reproduction in Magang goose ganders. Domest Anim Endocrinol 32, 190–200.CrossRefGoogle ScholarPubMed
Sugiyama, T, Minoura, H, Kawabe, N, Tanaka, M and Nakashima, K (1994). Preferential expression of long form prolactin receptor mRNA in the rat brain during the oestrous cycle, pregnancy and lactation: hormones involved in its gene expression. J Endocrinol 141, 325–33.10.1677/joe.0.1410325CrossRefGoogle ScholarPubMed
Telleria, CM, Parmer, TG, Zhong, L, Clarke, DL, Albarracin, CT, Duan, WR, Linzer, DI and Gibori, G (1997). The different forms of the prolactin receptor in the rat corpus luteum: developmental expression and hormonal regulation in pregnancy. Endocrinology 138, 4812–20.CrossRefGoogle ScholarPubMed
van Den Hurk, R, Dijkstra, G and De Jong, FH (2002). Enhanced serum oestrogen levels and highly steroidogenic, luteinized atretic follicles in the ovaries of the Djungarian hamster (Phodopus sungorus) kept under a short photoperiod from birth. Eur J Endocrinol 147, 701–10.CrossRefGoogle Scholar
Wang, C, Hsueh, AJW and Erickson, GF (1980). Prolactin inhibition of estrogen production by cultured rat granulosa cell. Mol Cell Endocrinol 20, 135–44.CrossRefGoogle Scholar
Xu, LX, Xue, HL, Li, SN, Xu, JH and Chen, L (2017). Seasonal differential expression of KiSS-1/GPR54 in the striped hamsters (Cricetulus barabensis) among different tissues. Integr Zool 12, 260–8.CrossRefGoogle ScholarPubMed
Xue, HL, Xu, JH, Chen, L and Xu, LX (2014). Genetic variation of the striped hamster (Cricetulus barabensis) and the impact of population density and environmental factors. Zoo Stud 53, 1–8.CrossRefGoogle Scholar
Yong, EL, Baird, DT and Hillier, SG (1992). Mediation of gonadotrophin-stimulated growth and differentiation of human granulosa cells by adenosine-3¢,5¢-monophosphate: one molecule, two messages. Clin Endocrinol (Oxf) 37, 51–8.CrossRefGoogle Scholar
Zhang, L, Li, DY, Liu, YP, Wang, Y, Zhao, XL and Zhu, Q (2012). Genetic effect of the prolactin receptor gene on egg production traits in chickens. Genet Mol Res 11, 4307–4315.CrossRefGoogle ScholarPubMed
Zhang, ZB and Wang, ZW (1998). Ecology and Control Strategies of Important Agricultural Rodent Pests. Beijing: Ocean Press.Google Scholar
Zhao, L, Zhong, M, Xue, HL, Ding, JS, Wang, S, Xu, JH, Lei, C and Xu, LX (2014). Effect of RFRP-3 on reproduction is sex- and developmental status-dependent in the striped hamster (Cricetulus barabensis). Gene 547, 273–9.CrossRefGoogle Scholar
Zhou, JF, Zadworny, D, Guémené, D and Kuhnlein, U (1996). Molecular cloning, tissue distribution, and expression of the prolactin receptor during various reproductive states in Meleagris gallopavo . Biol Reprod 55, 1081–90.CrossRefGoogle ScholarPubMed