Research Article
BibTex RIS Cite

Adult Male Syrian Hamsters (Mesocricetus auratus) Exhibit Daily Oscillations in Their Serum Levels of Melatonin and Leptin As Well As in the Expression of the GnRH, GnIH, and Kisspeptin Genes

Year 2023, Volume: 10 Issue: 1, 68 - 75, 28.01.2023
https://doi.org/10.30910/turkjans.1196793

Abstract

The complex neuronal and hormonal interaction between the brain and gonads controls the neuroendocrine reproductive axis. GnRH, GnIH, and kisspeptin are important neuropeptides in this relationship. Although seasonal variations of these neuropeptides have been demonstrated in photoperiodic animals, there is no clear evidence in their daily rhythms. Melatonin and leptin hormones are also two important hormones in reproductive regulation. In our study, the relationship of melatonin and leptin hormones with daily rhythm with GnIH, GnRH, and kisspeptin gene expressions and protein oscillations was examined. Adult male Syrian hamsters were exposed to the long photoperiod and at the end of the 30-day experimental period, blood and tissue samples from each group were collected at 04:00 h, 12:00 h, 20:00 h, and 00:00 h. Daily rhythms of melatonin and leptin hormones were determined by ELISA. Quantitative analysis of GnRH, GnIH, Kisspeptin, and β-actin genes was performed with the corresponding primers in Real-Time PCR. Protein expressions were determined by the Western Blot technique. Serum melatonin and leptin levels showed an inverse rhythmic relationship. Leptin level was found to be low while melatonin was high in the dark. Daily rhythms were observed in GnIH, GnRH, and kisspeptin mRNA expressions and protein oscillations. As a result, our findings could imply that all of the relationships between melatonin, leptin, GnIH, GnRH, and kisspeptin are not reproductive, but rather metabolic in nature.

Supporting Institution

Canakkale Onsekiz Mart Üniversity

Project Number

FDK-2021-3831

Thanks

This study was funded by the Scientific Research Projects Coordination Unit at Çanakkale Onsekiz Mart University (FDK-2021-3831)

References

  • Ahima, R.S., Prabakaran, D. and Flier, J.S. 1998. Postnatal leptin range and regulation of circadian rhythm of leptin by feeding implications for energy homeostasis and neuroendocrine function. Journal of Clinical Investigation, 101 (5): 1020-1027.
  • Bliss, S.P., Navratil, A.M., Xie, J. and Roberson, M.S. 2010. GnRH signaling, the gonadotrope and endocrine control of fertility. Neuroendocrinology, 31(3): 322-340.
  • Chehab, F.F., Lim, M. and Ronghua, L. 1996. Correction of sterility defect in omozygous obese female mice by treatment with the human recombinant leptin. Nature Genetics, 12 (3): 318–320.
  • Drazen, D.L., Kriegsfeld, L.J., Schneider, J.E. and Nelson, R.J. 2000. Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod. American Journal of Physiology, 278 (6): 1401-1407.
  • Guh, Y. J., Tamai, T. K. and Yoshimura, T. 2019. The underlying mechanisms of vertebrate seasonal reproduction. Proceedings of the Japan Academy, Series B, 95 (7): 343-357.
  • Gündüz, B. 2002. Daily rhythm in serum melatonin and leptin levels in the Syrian hamster (Mesocricetus auratus). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 132 (2): 393-401.
  • Gündüz, B. 2014. Serum leptin profiles, food intake, and body weight in melatonin-implanted Syrian hamsters (Mesocricetus auratus) exposed to long and short photoperiods. Turkish Journal of Biology, 38 (2): 185-192.
  • Hill, J.W, Elmquist, J.K. and Elias, C.F. 2008. Hypothalamic pathways linking energy balance and reproduction. American Journal Physiology Endocrinology Metabolism, 294 (5): 827-832
  • Hoffman, R. A. and Reiter, R. J. 1965. Pineal gland: influence on gonads of male hamsters. Science, 148 (3677): 1609-1611.
  • Johnson, M.A., Tsutsui, K. and Fraley, G.S. 2007. Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Hormones & Behaviour 51 (1): 171–180.
  • Kalsbeek, A., Fliers, E., Romijn, J. A., La Fleur, S. E., Wortel, J., Bakker, O. and Buijs, R. M. 2001. The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology, 142 (6): 2677-2685.
  • Karakas, A. and Gündüz, B. 2006. Suprachiasmatic nuclei may regulate the rhythm of leptin hormone release in Syrian hamsters (Mesocricetus auratus). Chronobiology international, 23 (1-2): 225-236.
  • Kawano, E., Takahata, Y., Oishi, T., Ukena, K., Tsutsui, K. and Tamotsu, S. 2006. Neural interaction of gonadotropin-regulating hormone immunoreactive neurons and the suprachiasmatic nucleus with the paraventricular organ in the Japanese grass lizard (Takydromus tachydromoides). Zoological Science, 23 (3): 277-287.
  • Klingenspor, M., Dickopp, A., Heldmaier, G. and Klaus, S., 1996. Short photoperiod reduces leptin gene expression in white and brown adipose tissue of Djungarian hamsters. FEBS Letters, 399 (3): 290–294.
  • Klingenspor, M., Niggemann, H. and Heldmaier, G., 2000. Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. Journal of Comparative Physiology B, 170 (1): 37–43.
  • Kriegsfeld, L. J., Mei, D. F., Bentley, G. E., Ubuka, T., Mason, A. O., Inoue, K. and Silver, R. 2006. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proceedings of the National Academy of Sciences, 103 (7): 2410-2415.
  • Li, Q., Rao, A., Pereira, A., Clarke, I. J. and Smith, J. T. 2011. Kisspeptin cells in the ovine arcuate nucleus express prolactin receptor but not melatonin receptor. Journal of Neuroendocrinology, 23 (10): 871-882.
  • Masson-Pévet, M., George, D., Kalsbeek, A., Saboureau, M., Lakhadar-Ghazal, N. and Pevet, P. 1994. An attempt to correlate brain areas containing melatonin-binding sites with rhythmic functions: a study in five hibernator species. Cell and tissue research, 278 (1): 97-106.
  • Maywood, E. S. and Hastings, M. H. 1995. Lesions of the iodomelatonin-binding sites of the mediobasal hypothalamus spare the lactotropic but block the gonadotropic response of male Syrian hamsters to short photoperiod and to melatonin. Endocrinology, 136(1): 144-153.
  • Navarro, V. M., Gottsch, M. L., Chavkin, C., Okamura, H., Clifton, D. K. and Steiner, R. A. 2009. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. Journal of Neuroscience, 29(38): 11859-11866.
  • Reiter, R.J. 1993. The melatonin rhythm: both a clock and a calendar. Experientia, 49(8): 654–664.
  • Silverman, A. J. 1988. The gonadotropin-releasing hormone (GnRH) neuronal systems: immunocytochemistry. The Physiology of Reproduction. Smith, J. T., Clifton, D. K. and Steiner, R. A. 2006. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction, 131 (4): 623-630.
  • Tsutsui, K., Bentley, G.E., Ubuka, T., Saigoh, E., Yin, H., Osugi, T., Inoue, K., Chowdhury, V.S., Ukena, K., Ciccone, N., Sharp, P.J. and Wingfield, J.C. 2007. The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). General and Comparative Endocrinology, 153 (1-3): 365-370.
  • Tsutsui, K., Saigoh, E., Ukena, K., Teranishi, H., Fujisawa, Y., Kikuchi, M., Ishii, S. and Sharp, P.J. 2000. A novel avianhypothalamic peptide inhibiting gonadotropin release. Biochemical and Biophysical Research Communications, 275 (2): 661–667.
  • Ubuka, T., Morgan, K., Pawson, A. J., Osugi, T., Chowdhury, V. S., Minakata, H. and Bentley, G. E. 2009. Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. Plos One, 4 (12): 8400.
  • Wade, G.N., Schneider, J.E. and Li H.Y. 1996. Control of fertility by metabolic cues. American Journal of Physiology, 270 (1): 1–19.

Yetişkin Erkek Suriye Hamsterleri (Mesocricetus auratus), Serum Melatonin ve Leptin Seviyelerinde ve Ayrıca GnRH, GnIH ve Kisspeptin Genlerinin Ekspresyonunda Günlük Ritim Gösterir

Year 2023, Volume: 10 Issue: 1, 68 - 75, 28.01.2023
https://doi.org/10.30910/turkjans.1196793

Abstract

Nöroendokrin ve üreme sistemi beyin ve gonadlar arasındaki kompleks nöronal ve hormonal etkileşim ile kontrol edilmektedir. GnRH, GnIH ve Kisspeptin bu ilişkide önemli nöropeptidlerdir. Bu nöropeptitlerin mevsimsel olarak değişimleri fotoperiyodik hayvanlarda gösterilmiş olsa da, günlük ritimlerinde net bir bilgi bulunmamaktadır. Ayrıca, melatonin ve leptin hormonları da üremenin düzenlenmesinde önemli iki hormondur. Çalışmamızda günlük melatonin ve leptin ritimlerinin GnIH, GnRH ve kisspeptin gen ekspresyonları ve protein salınımları ile ilişkisi incelendi. Yetişkin erkek Suriye hamsterleri uzun fotoperiyotta tutuldular. 30 günlük deney süresinin sonunda her gruptan günün 04:00, 12:00, 20:00 ve 00:00 saatlerinde kan ve doku örnekleri alındı. Melatonin ve leptin hormonlarının günlük ritimleri ELISA ile belirlendi. Real Time PCR yöntemiyle GnRH, GnIH, kisspeptin ve β-aktin genlerine karşılık gelen primerler kullanılarak bu genlerin kantitatif analizi yapıldı. Protein ifadeleri Western Blot tekniği ile belirlendi. Serum melatonin ve leptin seviyeleri ters yönlü ritmik ilişki gösterdi. Karanlıkta leptin düzeyi düşük, melatonin düzeyi yüksek bulundu. GnIH, GnRH ve Kisspeptin mRNA ifadelerinde ve protein salınımlarında günlük ritimler gözlendi. Sonuç olarak bulgularımız, melatonin, leptin, GnIH, GnRH ve kisspeptin arasındaki ilişkilerin üreme üzerinde olmayabileceği ancak metabolik olabileceğini düşündürmektedir

Project Number

FDK-2021-3831

References

  • Ahima, R.S., Prabakaran, D. and Flier, J.S. 1998. Postnatal leptin range and regulation of circadian rhythm of leptin by feeding implications for energy homeostasis and neuroendocrine function. Journal of Clinical Investigation, 101 (5): 1020-1027.
  • Bliss, S.P., Navratil, A.M., Xie, J. and Roberson, M.S. 2010. GnRH signaling, the gonadotrope and endocrine control of fertility. Neuroendocrinology, 31(3): 322-340.
  • Chehab, F.F., Lim, M. and Ronghua, L. 1996. Correction of sterility defect in omozygous obese female mice by treatment with the human recombinant leptin. Nature Genetics, 12 (3): 318–320.
  • Drazen, D.L., Kriegsfeld, L.J., Schneider, J.E. and Nelson, R.J. 2000. Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod. American Journal of Physiology, 278 (6): 1401-1407.
  • Guh, Y. J., Tamai, T. K. and Yoshimura, T. 2019. The underlying mechanisms of vertebrate seasonal reproduction. Proceedings of the Japan Academy, Series B, 95 (7): 343-357.
  • Gündüz, B. 2002. Daily rhythm in serum melatonin and leptin levels in the Syrian hamster (Mesocricetus auratus). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 132 (2): 393-401.
  • Gündüz, B. 2014. Serum leptin profiles, food intake, and body weight in melatonin-implanted Syrian hamsters (Mesocricetus auratus) exposed to long and short photoperiods. Turkish Journal of Biology, 38 (2): 185-192.
  • Hill, J.W, Elmquist, J.K. and Elias, C.F. 2008. Hypothalamic pathways linking energy balance and reproduction. American Journal Physiology Endocrinology Metabolism, 294 (5): 827-832
  • Hoffman, R. A. and Reiter, R. J. 1965. Pineal gland: influence on gonads of male hamsters. Science, 148 (3677): 1609-1611.
  • Johnson, M.A., Tsutsui, K. and Fraley, G.S. 2007. Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Hormones & Behaviour 51 (1): 171–180.
  • Kalsbeek, A., Fliers, E., Romijn, J. A., La Fleur, S. E., Wortel, J., Bakker, O. and Buijs, R. M. 2001. The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology, 142 (6): 2677-2685.
  • Karakas, A. and Gündüz, B. 2006. Suprachiasmatic nuclei may regulate the rhythm of leptin hormone release in Syrian hamsters (Mesocricetus auratus). Chronobiology international, 23 (1-2): 225-236.
  • Kawano, E., Takahata, Y., Oishi, T., Ukena, K., Tsutsui, K. and Tamotsu, S. 2006. Neural interaction of gonadotropin-regulating hormone immunoreactive neurons and the suprachiasmatic nucleus with the paraventricular organ in the Japanese grass lizard (Takydromus tachydromoides). Zoological Science, 23 (3): 277-287.
  • Klingenspor, M., Dickopp, A., Heldmaier, G. and Klaus, S., 1996. Short photoperiod reduces leptin gene expression in white and brown adipose tissue of Djungarian hamsters. FEBS Letters, 399 (3): 290–294.
  • Klingenspor, M., Niggemann, H. and Heldmaier, G., 2000. Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. Journal of Comparative Physiology B, 170 (1): 37–43.
  • Kriegsfeld, L. J., Mei, D. F., Bentley, G. E., Ubuka, T., Mason, A. O., Inoue, K. and Silver, R. 2006. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proceedings of the National Academy of Sciences, 103 (7): 2410-2415.
  • Li, Q., Rao, A., Pereira, A., Clarke, I. J. and Smith, J. T. 2011. Kisspeptin cells in the ovine arcuate nucleus express prolactin receptor but not melatonin receptor. Journal of Neuroendocrinology, 23 (10): 871-882.
  • Masson-Pévet, M., George, D., Kalsbeek, A., Saboureau, M., Lakhadar-Ghazal, N. and Pevet, P. 1994. An attempt to correlate brain areas containing melatonin-binding sites with rhythmic functions: a study in five hibernator species. Cell and tissue research, 278 (1): 97-106.
  • Maywood, E. S. and Hastings, M. H. 1995. Lesions of the iodomelatonin-binding sites of the mediobasal hypothalamus spare the lactotropic but block the gonadotropic response of male Syrian hamsters to short photoperiod and to melatonin. Endocrinology, 136(1): 144-153.
  • Navarro, V. M., Gottsch, M. L., Chavkin, C., Okamura, H., Clifton, D. K. and Steiner, R. A. 2009. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. Journal of Neuroscience, 29(38): 11859-11866.
  • Reiter, R.J. 1993. The melatonin rhythm: both a clock and a calendar. Experientia, 49(8): 654–664.
  • Silverman, A. J. 1988. The gonadotropin-releasing hormone (GnRH) neuronal systems: immunocytochemistry. The Physiology of Reproduction. Smith, J. T., Clifton, D. K. and Steiner, R. A. 2006. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction, 131 (4): 623-630.
  • Tsutsui, K., Bentley, G.E., Ubuka, T., Saigoh, E., Yin, H., Osugi, T., Inoue, K., Chowdhury, V.S., Ukena, K., Ciccone, N., Sharp, P.J. and Wingfield, J.C. 2007. The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). General and Comparative Endocrinology, 153 (1-3): 365-370.
  • Tsutsui, K., Saigoh, E., Ukena, K., Teranishi, H., Fujisawa, Y., Kikuchi, M., Ishii, S. and Sharp, P.J. 2000. A novel avianhypothalamic peptide inhibiting gonadotropin release. Biochemical and Biophysical Research Communications, 275 (2): 661–667.
  • Ubuka, T., Morgan, K., Pawson, A. J., Osugi, T., Chowdhury, V. S., Minakata, H. and Bentley, G. E. 2009. Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. Plos One, 4 (12): 8400.
  • Wade, G.N., Schneider, J.E. and Li H.Y. 1996. Control of fertility by metabolic cues. American Journal of Physiology, 270 (1): 1–19.
There are 26 citations in total.

Details

Primary Language English
Journal Section Research Article
Authors

Emine İnci Balkan 0000-0002-2708-2427

Bülent Gündüz 0000-0003-0497-8287

Project Number FDK-2021-3831
Publication Date January 28, 2023
Submission Date October 31, 2022
Published in Issue Year 2023 Volume: 10 Issue: 1

Cite

APA Balkan, E. İ., & Gündüz, B. (2023). Adult Male Syrian Hamsters (Mesocricetus auratus) Exhibit Daily Oscillations in Their Serum Levels of Melatonin and Leptin As Well As in the Expression of the GnRH, GnIH, and Kisspeptin Genes. Turkish Journal of Agricultural and Natural Sciences, 10(1), 68-75. https://doi.org/10.30910/turkjans.1196793