Besin Kısıtlaması Uygulanan Suprakiazmatik Nükleus Lezyonlu Gerbillerde (Meriones unguiculatus) Sirkadiyen Ritim ve Leptin Hormon Yanıtları

Yıl 2023, Cilt: 7 Sayı: 2, 119 - 126, 31.12.2023

Bülent Gündüz , Betül Önder , Ahmet Ekin , Nursel Hasanoğlu Akbulut

https://doi.org/10.31594/commagene.1378509

Öz

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.

Anahtar Kelimeler

Aktivite, vücut ağırlığı, biyolojik saat, beslenme

Etik Beyan

Araştırma için yasal etik kurul onayı izinleri Çanakkale Onsekiz Mart Üniversitesi Hayvan Deneyleri Yerel Etik Kurulu'ndan (No: 2011/08-03) alınmıştır.

Destekleyen Kurum

Çanakkale Onsekiz Mart Üniversitesi Bilimsel Araştırma Projesi

Proje Numarası

BAP- 2012/051

Circadian Rhythm and Leptin Hormone Responses to Nutritional Restriction in Gerbils (Meriones unguiculatus) with Suprachiasmatic Nucleus Lesions

Öz

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.

Anahtar Kelimeler

Activity, body weight, biological clock, feeding

Etik Beyan

This study was performed in accordance with ethical standards of animal experiments. Legal research ethics committee approval permissions for the study were obtained from the Canakkale Onsekiz Mart University, Animal Experiments Local Ethics Committee (No: 2011/08-03).

Destekleyen Kurum

Directory of Scientific Research Projects of Canakkale Onsekiz Mart University

Proje Numarası

BAP- 2012/051

Kaynakça

• 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
• 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
• 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
• 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
• 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
• Colwell, C.S., Witkovsky, P., & Silver, R. (2015). The suprachiasmatic nucleus (SCN): Critical points. In: Colwell CS (Ed.) Circadian Medicine. Wiley Blackwell, 37-55.
• 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
• 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
• 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
• 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
• 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
• 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
• 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., & 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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.
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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.
• 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
• 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
• 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
• 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