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RFRP-3 synchronized with photoperiods regulates the seasonal reproduction of striped hamsters

Published online by Cambridge University Press:  01 December 2021

Huiliang Xue
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong, 273165, China
Jinhui Xu
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong, 273165, China
Lei Chen
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong, 273165, China
Lei Zhao
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong, 273165, China
Ming Wu
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong, 273165, China
Laixiang Xu*
Affiliation:
College of Life Sciences, Qufu Normal University, Qufu, Shandong, 273165, China
*
Author for correspondence: Laixiang Xu. College of Life Sciences, Qufu Normal University, 57 Jingxuan West Road, Qufu, Shandong, 273165, China. E-mail: xulx@qfnu.edu.cn

Summary

The purpose of this study was to investigate the effect of RFRP-3 synchronized with photoperiods on regulating the seasonal reproduction of striped hamsters. The striped hamsters were raised separately under long-day (LD; 16 h light/8 h dark), medium-day (MD; 12 h light/12 h dark) or short-day (SD; 8 h light/16 h dark) conditions for 8 weeks. RFRP-3 and gonadotropin-releasing hormone (GnRH) mRNA levels in the hypothalamus, testis or ovaries in three groups were detected using reverse transcription polymerase chain reaction (RT-PCR). Melatonin (MLT), follicle-stimulating hormone (FSH) and luteinizing hormone (LH) concentrations in serum were detected using enzyme-linked immunosorbent assay (ELISA). The correlation between RFRP-3 and GnRH mRNA and FSH and LH concentrations was also analyzed. MLT negatively regulated the expression of RFRP-3. Significant differences for RFRP-3 mRNA existed in the three groups, which positively correlated with the GnRH and the FSH and LH concentrations. RFRP-3 mRNA levels in the hypothalamus were significantly higher than those in ovaries or testis. RFRP-3 levels in the hypothalamus were significantly lower in female than in male under SD conditions, while those in ovaries were significantly higher than those in testes under LD conditions. MLT decreased RFRP neuron activity, and RFRP-3 regulated the reproduction of striped hamsters.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Bronson, FH (1989). Mammalian Reproductive Biology. Chicago: University of Chicago Press.Google Scholar
Clarke, IJ, Sari, IP, Qi, Y, Smith, JT, Parkington, HC, Ubuka, T, Iqbal, J, Li, Q, Tilbrook, A, Morgan, K, Pawson, AJ, Tsutsui, K, Millar, RP and Bentley, GE (2008). Potent action of RFRP-3 on pituitary gonadotropes indicative of an hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 149, 5811–21.CrossRefGoogle ScholarPubMed
Dardente, H, Birnie, M, Lincoln, GA and Hazlerigg, DG (2008). RFamide related peptide and its cognate receptor in the sheep: cDNA cloning, mRNA distribution in the hypothalamus and the effect of photoperiod. J Neuroendocrinol 20, 1252–9.CrossRefGoogle ScholarPubMed
Goldman, BD (2001). Mammalian photoperiodic system: Formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms 16, 283301.CrossRefGoogle ScholarPubMed
Hahn, JD and Coen, CW (2006). Comparative study of the sources of neuronal projections to the site of gonadotrophin-releasing hormone perikarya and to the anteroventral periventricular nucleus in female rats. J Comp Neurol 494, 190214.CrossRefGoogle Scholar
Helfer, G, Barrett, P and Morgan, PJ (2019). A unifying hypothesis for control of body weight and reproduction in seasonally breeding mammals. J Neuroendocrinol 31, e12680.CrossRefGoogle ScholarPubMed
Janati, A, Talbi, R, Klosen, P, Mikkelsen, JD, Magoul, R, Simonneaux, V and El Ouezzani, S (2013). Distribution and seasonal variation in hypothalamic RFamide peptides in a semidesert rodent, the jerboa. J Neuroendocrinol 25, 402–11.CrossRefGoogle Scholar
Kadokawa, H, Shibata, M, Tanaka, Y, Kojima, T, Matsumoto, K, Oshima, K and Yamamoto, N (2009). Bovine C-terminal octapeptide of RFamide-related peptide-3 suppresses luteinizing hormone (LH) secretion from the pituitary as well as pulsatile LH secretion in bovines. Domest Anim Endocrinol 36, 219–24.CrossRefGoogle ScholarPubMed
Kriegsfeld, LJ, Mei, DF, Bentley, GE, Ubuka, T, Mason, AO, Inoue, K, Ukena, K, Tsutsui, K and Silver, R (2006). Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA 103, 2410–5.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2 (−delta C(T)) method. Methods 25, 402–8.CrossRefGoogle Scholar
Luo, ZX, Chen, W and Gao, W (2000). Chinese Fauna Beast Gang. Retrieved from vol. VI. Beijing: Science Press, pp. 28–38.Google Scholar
Mason, AO, Duffy, S, Zhao, S, Ubuka, T, Bentley, GE, Tsutsui, K, Silver, R and Kriegsfeld, LJ (2010). Photoperiod and reproductive condition are associated with changes in RFamide-related peptide (RFRP) expression in Syrian hamsters (Mesocricetus auratus). J Biol Rhythms 25, 176–85.CrossRefGoogle Scholar
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
Murakami, M, Matsuzaki, T, Iwasa, T, Yasui, T, Irahara, M, Osugi, T and Tsutsui, K (2008). Hypophysiotropic role of RFamide-related peptide-3 (RFRP-3) in the inhibition of LH secretion in female rats. J Endocrinol 199, 105–12.CrossRefGoogle ScholarPubMed
Pitrosky, B and Pévet, P (1997). The photoperiodic response in Syrian hamsters depends upon a melatonin-driven rhythm of sensitivity to melatonin. Biol Signals 6(4–6), 264–71.CrossRefGoogle ScholarPubMed
Revel, FG, Saboureau, M, Pévet, P, Simonneaux, V and Mikkelsen, JD (2008) RFamide-related peptide gene is a melatonin-driven photoperiodic gene. Endocrinology 149, 902–12.CrossRefGoogle ScholarPubMed
Rizwan, MZ, Poling, MC, Corr, M, Cornes, PA, Augustine, RA, Quennell, JH, Kauffman, AS and Anderson, GM (2012). RFamide-related peptide-3 receptor gene expression in GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology 153, 3770–9.CrossRefGoogle ScholarPubMed
Rutledge, RG and Stewart, D (2008). A kinetic-based sigmoidal model for the polymerase chain reaction and its application to high-capacity absolute quantitative real-time PCR. BMC Biotechnol 8, 47.CrossRefGoogle ScholarPubMed
Sari, IP, Rao, A, Smith, JT, Tilbrook, AJ and Clarke, IJ (2009). Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology 150, 5549–56.CrossRefGoogle ScholarPubMed
Simonneaux, V and Ancel, C (2012). RFRP neurons are critical gate keepers for the photoperiodic control of reproduction. Front Endocrinol 3, 168.CrossRefGoogle Scholar
Simonneaux, V, Ancel, C, Poirel, VJ and Gauer, F. (2013). Kisspeptins and RFRP-3 act in concert to synchronize rodent reproduction with seasons. Front Neurosci 7, 22.CrossRefGoogle ScholarPubMed
Smith, JT and Clarke, IJ (2010). Gonadotropin inhibitory hormone function in mammals. Trends Endocrinol Metab 21, 255–60.CrossRefGoogle ScholarPubMed
Smith, JT, Coolen, LM, Kriegsfeld, LJ, Sari, IP, Jaafarzadehshirazi, MR, Maltby, M, Bateman, K, Goodman, RL, Tilbrook, AJ, Ubuka, T, Bentley, GE, Clarke, IJ and Lehman, MN (2008). Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 149, 5770–82.CrossRefGoogle ScholarPubMed
Ubuka, T, Bentley, GE, Ukena, K, Wingfield, JC and Tsutsui, K (2005). Melatonin induces the expression of gonadotropin- inhibitory hormone in the avian brain. Proc Natl Acad Sci USA 102, 3052–7.CrossRefGoogle ScholarPubMed
Ubuka, T, Inoue, K, Fukuda, Y, Mizuno, T, Ukena, K, Kriegsfeld, LJ and Tsutsui, K (2012). Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology 153, 373–85.CrossRefGoogle ScholarPubMed
Urbanski, HF, Doan, A and Pierce, M (1991). Immunocytochemical investigation of luteinizing hormone-releasing hormone neurons in Syrian hamsters maintained under long or short days. Biol Reprod 44, 687–92.CrossRefGoogle ScholarPubMed