TY - JOUR T1 - Circadian Rhythm and Leptin Hormone Responses to Nutritional Restriction in Gerbils (Meriones unguiculatus) with Suprachiasmatic Nucleus Lesions TT - Besin Kısıtlaması Uygulanan Suprakiazmatik Nükleus Lezyonlu Gerbillerde (Meriones unguiculatus) Sirkadiyen Ritim ve Leptin Hormon Yanıtları AU - Gündüz, Bülent AU - Önder, Betül AU - Ekin, Ahmet AU - Hasanoğlu Akbulut, Nursel PY - 2023 DA - December Y2 - 2023 DO - 10.31594/commagene.1378509 JF - Commagene Journal of Biology JO - Comm. J. Biol. PB - ABADER (Adıyaman Bilimsel Araştırmalar Derneği) WT - DergiPark SN - 2602-456X SP - 119 EP - 126 VL - 7 IS - 2 LA - en AB - Rhythmically-regulated feeding behavior is in harmony with physiologic and metabolic activities in mammals. This rhythmic regulation is orchestrated by Suprachiasmatic Nucleus (SCN). However, it is not entirely clear how the SCN, which generates endogenous (internal) rhythms, influences body weight and serum leptin profile with activity rhythms in relation to feeding timing. In this study, animals in long photoperiod (14L:10D) were divided into two groups as control (sham-SCNx) and SCN lesions (SCNx). Then, these groups were split into four separate subgroups: a) ad libitum feeding; b) feeding only during the dark phase; c) feeding only during the light phase; and d) feeding during a specific period of the day (11:00-14:00 h). Locomotor activity and leptin hormone changes were observed in animals fed in cages attached to activity wheels for one month. Under the conditions of food restriction, the locomotor activities of the groups with SCNx and sham-SCNx demonstrated a phase shift toward the time of feeding. Serum leptin level did not change with feeding conditions but decreased in lesioned groups (SCNx). In conclusion, nutritional restriction caused phase shifts in activity rhythms and it was found that the SCN in gerbils was in charge of these rhythmic changes in the presence and absence of nutrients. KW - Activity KW - body weight KW - biological clock KW - feeding N2 - Ritmik olarak düzenlenen beslenme davranışı, memelilerdeki fizyolojik ve metabolik aktivitelerle uyum içindedir. Bu ritmik düzenleme Suprakiyazmatik Nükleus (SCN) tarafından yönetilir. Ancak endojen (iç) ritimler üreten SCN'nin beslenme zamanlamasına bağlı olarak vücut ağırlığını ve serum leptin profilini aktivite ritimleriyle nasıl etkilediği tam olarak açık değildir. Bu çalışmada, uzun fotoperiyottaki (14L:10D) hayvanlar kontrol (sham-SCNx) ve SCN lezyonları (SCNx) olmak üzere iki gruba ayrıldı. Daha sonra bu gruplar a) Ad libitum; b) Sadece gece fazında beslenme; c) Sadece gündüz fazında beslenme ve d) Günün belirli bir zamanında (11:00-14:00) beslenme olmak üzere dört ayrı alt gruba ayrıldı. Bir ay boyunca aktivite tekerleklerine bağlı kafeslerde beslenen hayvanlarda lokomotor aktivite ve leptin hormonu değişiklikleri gözlendi. Besin kısıtlaması koşulları altında, SCNx ve sham-SCNx'li grupların lokomotor aktiviteleri, beslenme zamanına doğru bir faz kayması göstermiştir. Serum leptin düzeyi beslenme koşullarına göre değişmedi ancak lezyonlu gruplarda (SCNx) azalmıştır. Sonuç olarak, beslenme kısıtlamasının aktivite ritimlerinde faz kaymalarına neden olduğu ve gerbillerde SCN'nin besin varlığında ve yokluğunda bu ritmik değişikliklerden sorumlu olduğu belirlendi. CR - Abe, H., Honma, S., & Honma, K.I. (2007). Daily restricted feeding resets the circadian clock in the suprachiasmatic nucleus of CS mice. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 292(1), 607–615. https://doi.org/10.1152/ajpregu.00331.2006 CR - Acosta-Galvan, G., Yi, C.X., Van Der Vliet, J., Jhamandas, J. H., Panula, P. Angeles-Castellanos, M., …………. & Buijs, R.M. (2011). Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behaviour. Proceedings of the National Academy of Sciences of the United States of America, 108(14), 5813–5818. https://doi.org/10.1073/pnas.1015551108 CR - Caba, M., & Mendoza, J. (2018). Food-anticipatory behavior in neonatal rabbits and rodents: An update on the role of clock genes. Frontiers in Endocrinology, 9, 266. https://doi.org/10.3389/fendo.2018.00266 CR - Chabot, C.C., Connolly, D.M., & Waring, B.B. (2012). The effects of lighting conditions and food restriction paradigms on locomotor activity of common spiny mice, Acomys cahirinus. Journal of Circadian Rhythms, 10(6). https://doi.org/10.1186/1740-3391-10-6 CR - Challet, E., Pévet, P., Vivien-Roels, B., & Malan, A. (1997). Phase-advanced daily rhythms of melatonin, body temperature, and locomotor activity in food-restricted rats fed during daytime. Journal of Circadian Rhythms, 12(1), 65–79. https://doi.org/10.1177/074873049701200108 CR - Colwell, C.S., Witkovsky, P., & Silver, R. (2015). The suprachiasmatic nucleus (SCN): Critical points. In: Colwell CS (Ed.) Circadian Medicine. Wiley Blackwell, 37-55. CR - Couce, M.E., Burguera, B., Parisi, J.E., Jensen, M.D., & Lloyd, R.V. (1997). Localization of leptin receptor in the human brain. Neuroendocrinology, 66(3), 145–150. https://doi.org/10.1159/000127232 CR - Damiola, F., Le Minli, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U. (2000). Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes and Development, 14(23), 2950–2961. https://doi.org/10.1101/gad.183500 CR - Davidson, A.J., Cappendijk, S.L., & Stephan, F.K. (2000). Feeding-entrained circadian rhythms are attenuated by lesions of the parabrachial region in rats. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 278(5), R1296-R1304 CR - Davidson, A.J., Poole, A.S., Yamazaki, S., & Menaker, M. (2003). Is the food-entrainable circadian oscillator in the digestive system? Genes, Brain and Behavior, 2(1), 32-39 CR - De Araujo, L.D., Roa, S. L., Bueno, A.C., Coeli-Lacchini, F.B., Martins, C.S., Uchoa, E.T., ………… & De Castro, M. (2016). Restricted feeding schedules modulate in a different manner the expression of clock genes in rat hypothalamic nuclei. Frontiers in Neuroscience, 10. https://doi.org/10.3389/fnins.2016.00567 CR - Guan, X. M., Hess, J. F., Yu, H., Hey, P. J., & Van Der Ploeg, L.H.T. (1997). Differential expression of mRNA for leptin receptor isoforms in the rat brain. Molecular and Cellular Endocrinology, 133(1), 1–7. https://doi.org/10.1016/S0303-7207(97)00138-X CR - 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. CR - Gündüz, B., & Karakaş, A. (2011). Leptin hormonunun Suriye hamsterlerinde (Mesocricetus auratus) lokomotor aktivite üzerine etkileri. Turkish Journal of Biology, 35(6), 727–734. https://doi.org/10.3906/biy-1008-63 CR - Guzmán-Ruiz, M., Saderi, N., Cazarez-Márquez, F., Guerrero-Vargas, N. N., Basualdo, M.C., Acosta-Galván, G., & Buijs, R.M. (2014). The suprachiasmatic nucleus changes the daily activity of the arcuate nucleus α-MSH neurons in male rats. Endocrinology, 155(2), 525–535. https://doi.org/10.1210/en.2013-1604 CR - Hara, R., Wan, K., Wakamatsu, H., Aida, R., Moriya, T., Akiyama, M., & Shibata, S. (2001). Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes to Cells, 6(3), 269–278. https://doi.org/10.1046/j.1365-2443.2001.00419.x CR - Hastings, M.H., Maywood, E.S., & Brancaccio, M. (2018). Generation of circadian rhythms in the suprachiasmatic nucleus. Nature Reviews Neuroscience, 19(8), 453–469. https://doi.org/10.1038/s41583-018-0026-z CR - Holmes, M.M., & Mistlberger, R.E. (2000). Food anticipatory activity and photic entrainment in food-restricted BALB/c mice. Physiology and Behavior, 68(5), 655–666. https://doi.org/10.1016/S0031-9384(99)00231-0 CR - Hurtado-Parrado, C., Cardona-Zea, Á., Arias-Higuera, M., Cifuentes, J., Muñoz, A., Rico, J. L., & Acevedo-Triana, C. (2019). Behavioral patterns of laboratory Mongolian gerbils by sex and housing condition: a case study with an emphasis on sleeping patterns. Journal of Veterinary Behavior, 30, 69–79. https://doi.org/10.1016/j.jveb.2018.12.004 CR - Inyushkin, A.N., Bhumbra, G. S., & Dyball, R.E. J. (2009). Leptin modulates spike coding in the rat suprachiasmatic nucleus. Journal of Neuroendocrinology, 21(8), 705–714. https://doi.org/10.1111/j.1365-2826.2009.01889.x CR - Inyushkin, A.N., Petrova, A.A., & Tkacheva, M.A. (2018). Effects of neuropeptide Y on the functional state of the afferent inputs from the arcuate nucleus to the suprachiasmatic nucleus in rats in vitro. Neuroscience and Behavioral Physiology, 48(4), 511–520. https://doi.org/10.1007/s11055-018-0593-5 CR - Kalsbeek, A., Fliers, E., Romijn, J. A., La Fleur, S. E., Wortel, J., Bakker, O., … & Buijs, R. M. (2001). The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology, 142(6), 2677–2685. https://doi.org/10.1210/endo.142.6.8197 CR - Karakaş, A., & Gündüz, B. (2006). Suprachiasmatic nuclei may regulate the rhythm of leptin hormone release in Syrian hamsters (Mesocricetus auratus). International Journal of Chronobiology, 23(1–2), 225–236. https://doi.org/10.1080/07420520500545821 CR - Karakaş, A., Serin, E., & Gündüz, B. (2006). Food restriction affects locomotor activity in Mongolian gerbils (Meriones unguiculatus). Turkish Journal of Biology, 30(1), 23–28. CR - Karakaş, A. (2011). The effects of photoperiod and age on food anticipatory activity in Mongolian gerbils (Meriones unguiculatus). Biological Rhythm Research, 42, no. 1, 53–65. https://doi.org/10.1080/09291011003729239 CR - Kettner, N.M., Mayo, S.A., Hua, J., Lee, C., Moore, D.D., & Fu, L. (2015). Circadian dysfunction induces leptin resistance in mice. Cell Metabolism, 22(3), 448–459. https://doi.org/10.1016/j.cmet.2015.06.005 CR - Klaus, U., Weinandy, R., & Gattermann, R. (2000). Circadian activity rhythms and sensitivity to noise in the Mongolian gerbil (Meriones unguiculatus). Chronobiology International, 17(2), 137–145. https://doi.org/10.1081/CBI-100101038 CR - Lamont, E.W., Renteria Diaz, L., Barry-Shaw, J., Stewart, J., & Amir, S. (2005). Daily restricted feeding rescues a rhythm of period2 expression in the arrhythmic suprachiasmatic nucleus. Neuroscience, 132(2), 245–248. https://doi.org/10.1016/j.neuroscience.2005.01.029 CR - Landry, G.J., Yamakawa, G.R.S., & Mistlberger, R.E. (2007). Robust food anticipatory circadian rhythms in rats with complete ablation of the thalamic paraventricular nucleus. Brain Research, 1141, 108-118. https://doi.org/10.1016/j.brainres.2007.01.032 CR - LeDuc, C.A., & Leibel, R.L. (2019). Auto-Regulation of Leptin Neurobiology. Cell Metabolism, 30(4), 614–616. https://doi.org/10.1016/j.cmet.2019.09.006 CR - Liu, C., Weaver, D.R., Jin, X., Shearman, L.P., Pieschl, R.L., Gribkoff, V.K. & Reppert, S.M. (1997). Molecular dissection of two distinct actions of melatonin on the suprachiasmatic circadian clock. Neuron, 19, 91-102. http://doi.org/10.1016/S0896-6273(00)80350-5 CR - Marchant, E.G., & Mistlberger, R.E. (1997). Anticipation and entrainment to feeding time in intact and SCN-ablated C57BL/6j mice. Brain Research, 765(2), 273-282. http://doi.org/10.1016/S0006-8993(97)00571-4 CR - Mendoza, J., Lopez Lopez, C., Revel, F.G., Jeanneau, K., Delerue, F., Prinssen, E.,..……& Grundschober, C. (2011). Dimorphic effects of leptin on the circadian and hypocretinergic systems of mice. Journal of Neuroendocrinology, 23(1), 28–38. https://doi.org/10.1111/j.1365-2826.2010.02072.x CR - Mieda, M. (2020). The central circadian clock of the suprachiasmatic nucleus as an ensemble of multiple oscillatory neurons. Neuroscience Research, 156, 24–31. https://doi.org/10.1016/j.neures.2019.08.003 Mistlberger, R.E. (2009). Food-anticipatory circadian rhythms: Concepts and methods. European Journal of Neuroscience, 30(9), 1718–1729. https://doi.org/10.1111/j.1460-9568.2009.06965.x CR - Mistlberger, R.E. (2011). Neurobiology of food anticipatory circadian rhythms. Physiology and Behavior, 104(4), 535–545. https://doi.org/10.1016/j.physbeh.2011.04.015 CR - Mistlberger, R.E., & Mumby, D. (1992). The limbic system and food-anticipatory circadian rhythms in the rat: ablation and dopamine blocking studies. Behavioural Brain Research, 47(2), 159-168. https://doi.org/10.1016/S0166-4328(05)80122-6 CR - Moore, R.Y., Speh, J. C., & Leak, R.K. (2002). Suprachiasmatic nucleus organization. Cell and Tissue Research, 309(1), 89–98. https://doi.org/10.1007/s00441-002-0575-2 CR - Mukherji, A., Kobiita, A., Damara, M., Misra, N., Meziane, H., Champy, M.F., & Chambon, P. (2015). Shifting eating to the circadian rest phase misaligns the peripheral clocks with the master SCN clock and leads to a metabolic syndrome. Proceedings of the National Academy of Sciences, 112(48), E6691-E6698 CR - Nováková, M., Polidarová, L., Sládek, M., & Sumová, A. (2011). Restricted feeding regime affects clock gene expression profiles in the suprachiasmatic nucleus of rats exposed to constant light. Neuroscience, 197, 65–71. https://doi.org/10.1016/j.neuroscience.2011.09.028 CR - Nováková, M., Sládek, M., & Sumová, A. (2010). Exposure of pregnant rats to restricted feeding schedule synchronizes the SCN clocks of their fetuses under constant light but not under a light-dark regime. Journal of Biological Rhythms, 25(5), 350–360. https://doi.org/10.1177/0748730410377967 CR - Prosser, R.A., & Bergeron, H.E. (2003). Leptin phase-advances the rat suprachiasmatic circadian clock in vitro. Neuroscience Letters, 336(3), 139–142. https://doi.org/10.1016/S0304-3940(02)01234-X CR - Queiroz, J. do N., Macedo, R.C.O., Tinsley, G.M., & Reischak-Oliveira, A. (2021). Time-restricted eating and circadian rhythms: the biological clock is ticking. Critical Reviews in Food Science and Nutrition, 61(17), 2863-2875. https://doi.org/10.1080/10408398.2020.1789550 CR - Schibler,U., Ripperger, J., & Brown, S.S. (2003). Peripheral circadian oscillators in mammals: time and food. Journal of Biological Rhythms, 18(3), 250-260. https://doi.org/10.1177/0748730403018003007 CR - Stephan, F.K., Swann, J.M., & Sisk, C.L. (1979). Entrainment of circadian rhythms by feeding schedules in rats with suprachiasmatic nucleus lesions. Behavioral and Neural Biology, 25(4), 545-554. https://doi.org/10.1016/s0163-1047(79)90332-7. CR - Todd, W. D., Venner, A., Anaclet, C., Broadhurst, R. Y., De Luca, R., Bandaru, S.S., ………. & Fuller, P.M. (2020). Suprachiasmatic VIP neurons are required for normal circadian rhythmicity and comprised of molecularly distinct subpopulations. Nature Commununacations, 11(1), 1–20. https://doi.org/10.1038/s41467-020-17197-2 CR - Tso, C. F., Simon, T., Greenlaw, A. C., Puri, T., Mieda, M., & Herzog, E.D. (2017). Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behaviour. Current Biology, 27(7),1055–1061. https://doi.org/10.1016/j.cub.2017.02.037 CR - Weinert, D., Nevill, A., Weinandy, R., & Waterhouse, J. (2003). The development of new purification methods to assess the circadian rhythm of body temperature in Mongolian gerbils. Chronobiology International, 20(2), 249–270. https://doi.org/10.1081/CBI-120018649 CR - Zhang, S., Zeitzer, J.M., Yoshida, Y., Wisor, J.P., Nishino, S., Edgar, D.M., & Mignot, E. (2004). Lesions of the suprachiasmatic nucleus eliminate the daily rhythm of hypocretin-1 release. Sleep, 27(4), 619–627. https://doi.org/10.1093/sleep/27.4.619 UR - https://doi.org/10.31594/commagene.1378509 L1 - https://dergipark.org.tr/en/download/article-file/3485473 ER -