https://doi.org/10.4081/ejh.2023.3825

Seasonal patterns of prolactin, prolactin receptor, and STAT5 expression in the ovaries of wild ground squirrels (Citellus dauricus Brandt)

Vol. 67 No. 4 (2023)
Submitted: 10 July 2023
Accepted: 30 August 2023
Published: 2 October 2023
wild ground squirrel, prolactin, prolactin receptor, STAT5, ovary
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Authors

Qingjing Gao
Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.
Wenqian Xie
Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.
Wenjing Lu
Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.
Yuning Liu
Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.
Haolin Zhang
Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.
Yingying Han
Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.
Qiang Weng
qiangweng@bjfu.edu.cn
Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.

Prolactin (PRL) is a hormone crucial for normal reproduction, functioning as an autocrine, paracrine, and endocrine factor. This study aimed to examine the immunolocalization and expression patterns of PRL, prolactin receptor (PRLR), and signal transducer and activator of transcription 5 (STAT5) in the ovaries of wild ground squirrels during both breeding and non-breeding periods. Significant seasonal variations were observed in ovarian weights, with higher values during the breeding season and relatively lower values during the nonbreeding season. PRL, PRLR, STAT5, and p-STAT5 were immunolocalized in granulosa cells and luteal cells during the breeding season, whereas they were exclusively found in granulosa cells during the non-breeding season. The mRNA expression levels of Prl, Prlr, and Stat5 were increased in ovarian tissues during the breeding season compared to the non-breeding season. Moreover, the mean mRNA levels of Prl, Prlr, and Stat5 exhibited a positive correlation with ovarian weights. Both circulating PRL and ovarian PRL concentrations were significantly elevated during the breeding season. Additionally, transcriptomic analysis of ovarian tissues revealed differentially expressed genes possibly associated with ovarian function and mammary gland development, including ovarian follicle development, steroid synthesis, and regulation of reproductive process. These findings suggest that PRL might play an essential endocrine, autocrine, or paracrine role in the regulation of seasonal changes in the ovarian functions in wild ground squirrels.

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Citations

Crossref
Scopus
Google Scholar
Europe PMC
Freeman ME, Kanyicska B, Lerant A, Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol Rev 2000;80:1523-631. DOI: https://doi.org/10.1152/physrev.2000.80.4.1523
Bernichtein S, Touraine P, Goffin V. New concepts in prolactin biology. J Endocrinol 2010;206:1-11. DOI: https://doi.org/10.1677/JOE-10-0069
Horseman ND, Yu-Lee LY. Transcriptional regulation by the helix bundle peptide hormones: growth hormone, prolactin, and hematopoietic cytokines. Endocr Rev 1994;15:627-49. DOI: https://doi.org/10.1210/edrv-15-5-627
Bachelot A, Binart N. Reproductive role of prolactin. Reproduction 2007;133:361-9. DOI: https://doi.org/10.1530/REP-06-0299
Ben-Jonathan N, LaPensee CR, LaPensee EW. What can we learn from rodents about prolactin in humans? Endocr Rev 2008;29:1-41. DOI: https://doi.org/10.1210/er.2007-0017
Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 1998;19:225-68. DOI: https://doi.org/10.1210/edrv.19.3.0334
Clevenger CV, Furth PA, Hankinson SE, Schuler LA. The role of prolactin in mammary carcinoma. Endocr Rev 2003;24:1-27. DOI: https://doi.org/10.1210/er.2001-0036
Gao J, Hughes JP, Auperin B, Buteau H, Edery M, Zhuang H, et al. Interactions among Janus kinases and the prolactin (PRL) receptor in the regulation of a PRL response element. Mol Endocrinol 1996;10:847-56. DOI: https://doi.org/10.1210/mend.10.7.8813725
Hughes K, Watson CJ. The spectrum of STAT functions in mammary gland development. JAKSTAT 2012;1:151-8. DOI: https://doi.org/10.4161/jkst.19691
Qian L, Lopez V, Seo YA, Kelleher SL. Prolactin regulates ZNT2 expression through the JAK2/STAT5 signaling pathway in mammary cells. Am J Physiol Cell Physiol 2009;297:C369-77. DOI: https://doi.org/10.1152/ajpcell.00589.2008
Bridgewater RE, Streuli CH, Caswell PT. Extracellular matrix promotes clathrin-dependent endocytosis of prolactin and STAT5 activation in differentiating mammary epithelial cells. Sci Rep 2017;7:4572. DOI: https://doi.org/10.1038/s41598-017-04783-6
Harvey S, Martínez-Moreno CG, Luna M, Arámburo C. Autocrine/paracrine roles of extrapituitary growth hormone and prolactin in health and disease: An overview. Gen Comp Endocrinol 2015;220:103-11. DOI: https://doi.org/10.1016/j.ygcen.2014.11.004
Foitzik K, Langan EA, Paus R. Prolactin and the skin: a dermatological perspective on an ancient pleiotropic peptide hormone. J Invest Dermatol 2009;129:1071-87. DOI: https://doi.org/10.1038/jid.2008.348
Goffin V, Hoang DT, Bogorad RL, Nevalainen MT. Prolactin regulation of the prostate gland: a female player in a male game. Nat Rev Urol 2011;8:597607. DOI: https://doi.org/10.1038/nrurol.2011.143
Hair WM, Gubbay O, Jabbour HN, Lincoln GA. Prolactin receptor expression in human testis and accessory tissues: localization and function. Mol Hum Reprod 2002;8:606-11. DOI: https://doi.org/10.1093/molehr/8.7.606
Marano RJ, Ben-Jonathan N. Minireview: Extrapituitary prolactin: an update on the distribution, regulation, and functions. Mol Endocrinol 2014;28:622-33. DOI: https://doi.org/10.1210/me.2013-1349
Parks JS. Hormones of the hypothalamus and pituitary. Elsevier; 2004. p. 1845-69.
Horseman ND, Zhao W, Tanaka M, Nakashima K, Engle SJ, Smith F, et al. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. Embo J 2014;16:6926-35. DOI: https://doi.org/10.1093/emboj/16.23.6926
Liu X, Robinson GW, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L. Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev 1997;11:179-86. DOI: https://doi.org/10.1101/gad.11.2.179
Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 1997;11:167-78. DOI: https://doi.org/10.1101/gad.11.2.167
Tenorio Fd, Simões Mde J, Teixeira VW, Teixeira ÁA. Effects of melatonin and prolactin in reproduction: review of literature. Rev Assoc Med Bras (1992) 2015;61:269-74. DOI: https://doi.org/10.1590/1806-9282.61.03.269
Fan S, Lu W, Zhang H, Yuan Z, Han Y, Weng Q. Seasonal change in adiponectin associated with ovarian morphology and function in wild ground squirrels (Citellus dauricus Brandt). Int J Mol Sci 2022;23:14698. DOI: https://doi.org/10.3390/ijms232314698
Zhang H, Sheng X, Hu X, Li X, Xu H, Zhang M, et al. Seasonal changes in spermatogenesis and immunolocalization of cytochrome P450 17alpha-hydroxylase/c17-20. lyase and cytochrome P450 aromatase in the wild male ground squirrel (Citellus dauricus Brandt). J Reprod Dev 2010;56:297-302. DOI: https://doi.org/10.1262/jrd.09-078T
Li X, Zhang H, Sheng X, Li B, Zhou J, Xu M, et al. 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. DOI: https://doi.org/10.1186/1757-2215-5-26
Li B, Sheng X, Bao L, Huang S, Li Q, Liu Y,et al. Seasonal changes in expression of nerve growth factor and its receptors TrkA and p75 in the ovary of wild ground squirrel (Citellus dauricus Brandt). J Ovarian Res 2014;7:3. DOI: https://doi.org/10.1186/1757-2215-7-3
Bao L, Li Q, Liu Y, Li B, Sheng X, Han Y, et al. Immunolocalization of NGF and its receptors in ovarian surface epithelium of the wild ground squirrel during the breeding and nonbreeding seasons. Eur J Histochem 2014;58:2363. DOI: https://doi.org/10.4081/ejh.2014.2363
Li B, Sheng X, Song M, Zhang H, Weng J, Zhang M, et al. Expression of nerve growth factor and its receptors TrkA and p75 in the uterus of wild female ground squirrel (Citellus dauricus Brandt). Gen Comp Endocrinol 2012;176:62-9. DOI: https://doi.org/10.1016/j.ygcen.2011.12.024
Xie W, Liu H, Liu Q, Gao Q, Gao F, Han Y, et al. Seasonal expressions of prolactin, prolactin receptor and STAT5 in the scented glands of the male muskrats (Ondatra zibethicus). Eur J Histochem 2019;63:2991. DOI: https://doi.org/10.4081/ejh.2019.2991
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014;15:550. DOI: https://doi.org/10.1186/s13059-014-0550-8
Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2010;11:R14. DOI: https://doi.org/10.1186/gb-2010-11-2-r14
Zhang H, Wang Y, Zhang J, Wang L, Li Q, Sheng X, et al. Testicular expression of NGF, TrkA and p75 during seasonal spermatogenesis of the wild ground squirrel (Citellus dauricus Brandt). Eur J Histochem 2015;59:2522. DOI: https://doi.org/10.4081/ejh.2015.2522
Wang Y, Wang Z, Yu W, Sheng X, Zhang H, Han Y, et al. Seasonal expressions of androgen receptor, estrogen receptors and cytochrome P450 aromatase in the uteri of the wild Daurian ground squirrels (Spermophilus dauricus). Eur J Histochem 2018;62:2889. DOI: https://doi.org/10.4081/ejh.2018.2889
Lincoln G.A. Significance of seasonal cycles in prolactin secretion in male mammals, in: Serio M., Raven Press (Ed.), Perspectives in Andrology (Serono Symposia Publications), New York 1989;53:299–306.
Regisford EG, Katz LS. Effects of bromocriptine-induced hypoprolactinaemia on gonadotrophin secretion and testicular function in rams (Ovis aries) during two seasons. J Reprod Fertil 1993;99:529-37. DOI: https://doi.org/10.1530/jrf.0.0990529
Gloria E, Regisford C, Katz LS. Effects of bromocriptine treatment on the expression of sexual behavior in male sheep (Ovis aries). J Anim Sci 1994;72:591-7. DOI: https://doi.org/10.2527/1994.723591x
Xie W, Tang Z, Guo Y, Zhang C, Zhang H, Han Y, et al. Seasonal expressions of growth hormone receptor, insulin-like growth factor 1 and insulin-like growth factor 1 receptor in the scented glands of the muskrats (Ondatra zibethicus). Gen Comp Endocrinol 2019;281:58-66. DOI: https://doi.org/10.1016/j.ygcen.2019.05.014
Basini G, Baioni L, Bussolati S, Grolli S, Grasselli F. Prolactin is a potential physiological modulator of swine ovarian follicle function. Regul Pept 2014;189:22-30. DOI: https://doi.org/10.1016/j.regpep.2014.01.003
Binart N, Bachelot A, Bouilly J. Impact of prolactin receptor isoforms on reproduction. Trends Endocrinol Metab 2010;21:362-8. DOI: https://doi.org/10.1016/j.tem.2010.01.008
Picazo RA, García Ruiz JP, Santiago Moreno J, González de Bulnes A, Muñoz J, Silván G, et al. Cellular localization and changes in expression of prolactin receptor isoforms in sheep ovary throughout the estrous cycle. Reproduction 2004;128:545-53. DOI: https://doi.org/10.1530/rep.1.00343
Roy SK, Greenwald GS. In vitro effects of follicle-stimulating hormone, luteinizing hormone, and prolactin on follicular deoxyribonucleic acid synthesis in the hamster. Endocrinology 1988;122:952-8. DOI: https://doi.org/10.1210/endo-122-3-952
Hu, S. Zadworny, D. Effects of nonglycosylated and glycosylated prolactin on basal and gonadotropin-stimulated steroidogenesis in chicken ovarian follicles. Domest Anim Endocrinol 2017;61:27-38. DOI: https://doi.org/10.1016/j.domaniend.2017.05.002
Risk M, Gibori G. Mechanisms of luteal cell regulation by prolactin. In: Horseman ND (ed.) Prolactin. Springer, New York; 2001. pp 265-95. DOI: https://doi.org/10.1007/978-1-4615-1683-5_14
Ciereszko RE, Petroff BK, Ottobre AC, Guan Z, Stokes BT, Ottbre JS. Assessment of the mechanism by which prolactin stimulates progesterone production by early corpora lutea of pigs. J Endocrinol 1998;159:201-9. DOI: https://doi.org/10.1677/joe.0.1590201
Shibaya M, Murakami S, Tatsukawa Y, Skarzynski DJ, Acosta TJ, Okuda K. Bovine corpus luteum is an extrapituitary site of prolactin production. Mol Reprod Dev 2006;73:512-9. DOI: https://doi.org/10.1002/mrd.20445
Yang X, Friedl A. A positive feedback loop between prolactin and STAT5 promotes angiogenesis. Adv Exp Med Biol 2015;846:265-80. DOI: https://doi.org/10.1007/978-3-319-12114-7_12

Ethics Approval

All animal testing procedures were approved by the Animal Protection and Utilization Policy of the Beijing Forestry University Ethics Committee and approved by the Hebei Provincial Department of Agriculture

Supporting Agencies

Beijing Natural Science Foundation, National Natural Science Foundation of China

How to Cite

Gao, Q., Xie, W., Lu, W., Liu, Y., Zhang, H., Han, Y., & Weng, Q. (2023). Seasonal patterns of prolactin, prolactin receptor, and STAT5 expression in the ovaries of wild ground squirrels (<em>Citellus dauricus</em> Brandt). European Journal of Histochemistry, 67(4). https://doi.org/10.4081/ejh.2023.3825
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