Food, not the photoperiod, entrains the circadian rhythms in the liver of Winstar albino rats
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Abstract
The central oscillator is located in mammals' suprachiasmatic nucleus (SCN). The liver is the non-photic organ and the centre for metabolic activities. Food could be a potential zeitgeber for the liver as the timing of feeding is precise in animals. The present study hypothesized that the food provided at a different time of the day (consistently delay of 6 hours) could lead to the desynchronization of daily rhythms in clock genes in liver tissues. The Winstar albino rats were divided into three groups and were exposed to a daily light-dark cycle (12L:12D; 12h light and 12h dark). The Group 1 (Control group) had food ad libitum, Group 2- second group- 6h food group had daily food availability of 6h (night fed group). In contrast, Group 3- T30 group was provided food for 6 hours but delayed by 6h from the previous day's food timing. After 30 days, animals were sacrificed at six-time points and the expression of clock genes was studied in the liver. Food cycle's effect was observed on body mass, and it was significantly (P < 0.05) reduced in the T30 group. The circadian clock persisted in both food ad libitum and night fed groups but changed in phase and amplitude. However, it lost daily rhythm in clock genes in liver tissues of the T30 group. These results are significant as they suggest that the food's timing is critical for synchronizing the circadian clock in the metabolic center, i.e., the liver.
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Keywords
Circadian clock, Daily rhythms, Hepatic, Oscillation, Peripheral
References
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Balsalobre, A., Marcacc, L. & Schibler, U. (2000). Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Current Biology, 10, 1291–1294. https://doi.org/10.1016/S0960-9822(00)00758-2.
Borah, B. K., Renthlei, Z. & Trivedi, A. K. (2020). Hypothalamus but not liver retains daily expression of clock genes during hibernation in terai tree frog (Polypedates teraiensis). Chronobiology International, 37(4), 485–492. doi: 10.1080/07420528.2020.1726373.
Breno T. S. Carneiro, B. T. S., Fernandes, D. A. C., Medeiros, C. F. P., Diniz, N. L., Araujo, J. F. (2012). Daily anticipatory rhythms of behavior and body temperature in response to glucose availability in rats. Psychology & Neuroscience, 5(2), 191-197. doi.org/10.3922/j.psns.20 12.2.09.
Cassone, V. M. & Stephan, F. K. (2002). Central and peripheral regulation of feeding and nutrition by the mammalian circadian clock: implications for nutrition during manned space flight. Nutrition, 18(10), 814–819. doi.org/10.1016/S0899-9007(02)00937-1.
Challet, E., Caldelas, I., Graff, C. & Pevet, P. (2003). Synchronization of the molecular clockwork by light- and food-related cues in mammals. Biological Chemistry, 384, 711–719. doi: 10.1515/bc.2003.079. doi: 10.1515/BC.2003.079
Coleman, G. J., Harper, S., Clarke, J. D. & Armstrong, S. (1982). Evidence for a separate meal associated oscillator in the rat. Physiology and Behavior, 29, 107–115. https://doi.org/10.1016/0031-9384(82)90373-0.
Cox, K. H. & Takahashi, J. S. Circadian clock genes and the transcriptional architecture of the clock mechanism. Journal of Molecular Endocrinology, 63(4), R93-R102. doi: 10.1530/JME-19-0153. doi: 10.1530/JME-19-0153.
Cuesta, M., Clesse, D., Pe ́Vet, P. & Challet, E. (2009). From daily behaviour to hormonal and neurotransmitters rhythms: Comparison between diurnal and nocturnal rat species. Hormones and Behavior, 55, 338–347. doi.org/10.1016/j.yhbeh.2008.10.015.
Damiola, F., Le, Minh, 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, 2950–2961. doi: 10.1101/gad.183500.
Davidson, A. J., Aragona, B. J., Werner, R. M., Schroeder, E., Smith, J. C. & Stephan, F. K. Food anticipatory activity persists after olfactory bulb ablation in the rat. Physiology and Behavior, 72, 231–235. doi: 10.1016/s0031-9384(00)00417-0.
Dibner, C., Schibler, U. & Albrecht, U. (2010). The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annual Review of Physiology, 72, 517–549. doi: 10.1146/annurev-physiol-021909-135821.
Feillet, C. A., Mendoza, J., Pevet, P. & Challet, E. (2008). Restricted feeding restores rhythmicity in the pineal gland of arrhythmic suprachiasmatic-lesioned rats. European Journal of Neuroscience, 28, 2451–2458. doi: 10.1111/j.1460-9568.2008.06538.x.
Garaulet, M. & Gómez-Abellán, P. (2014). Timing of food intake and obesity: a novel association. Physiology and Behavior, 134, 44–50. doi: 10.1016/j.physbeh.20 14.0 1.001.
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, 269-278. doi: 10.1046/j.1365-2443.2001.00419.x.
Hernández-Pérez, J., Míguez, J. M., Naderi, F., Soengas, J. L. & López-Patiño, M. A. (2017). Influence of light and food on the circadian clock in liver of rainbow trout, Oncorhynchus mykiss. Chronobiology International, 34(9), 1259–1272. doi.org/10.1080/07420528.2017.1361435.
Honma, K., von Goetz, C. & Aschoff, J. (1983). Effects of restricted daily feeding on free running circadian rhythms in rats. Physiology and Behavior, 30, 905–913. doi.org/10.1016/0031-9384(83)90256-1.
Kamphuis, W., Cailotto, C., Dijk, F., Bergen, A. & Buijs, R. M. (2005). Circadian expression of clock genes and clock-controlled genesin the rat retina. Biochemical and Biophysical Research Communications, 330, 18–26. doi: 10.1016/j.bbrc.2005.02.118.
Kornmann, B., Preitner, N., Rifat, D., Fleury-Olela, F. & Schibler, U. (2001). Analysis of circadian liver gene expression by ADDER, a highly sensitive method for the display of differentially expressed mRNAs. Nucleic Acids Research, 29, E51– 51. doi: 10.1093/nar/29.11.e51.
Krizo,J. A., Moreland, L. E., Rastogi, A., Mou, X., Prosser, R. A., Mintz, E. A. (2018). Regulation of Locomotor activity in fed, fasted, and food-restricted mice lacking tissue-type plasminogen activator. BMC Physiology,18:2. doi: 10.1186/s12899-018-0036-0.
Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(–ddC(T)) method. Methods, 25, 402–408. doi: 10.1006/meth.2001.1262.
McHill, A. W., Phillips, A. J., Czeisler, C. A., Keating, L., Yee, K., Barger, L. K., Garaulet, M., Scheer, F. A. & Klerman, E. B. (2017). Later circadian timing of food intake is associated with increased body fat. American Journal of Clinical Nutrition, 106(5), 1213–1219. doi.org/10.3945/ajcn.117.161588.
Mendez, M. A., Popkin, B. M., Buckland, G., Schroder, H., Amiano, P., Barricarte, A., Huert, J. M., Quirós, R. J., Sánchez, M. J. & González, C. A. (2011). Alternative methods of accounting for underreporting and overreporting when measuring dietary intake–obesity relations. American Journal of Epidemiology, 173, 448–58. doi: 10.1093/aje/kwq380.
Mistlberger, R. E. (1994). Circadian food-anticipatory activity: formal models and physiological mechanisms. Neuroscience and Biobehavioral Reviews, 18, 171–195. doi.org/10.1016/0149-7634(94)90023-X.
Mistlberger, R. E. (1993). Effects of scheduled food and water access on circadian rhythms of hamsters in constant light, dark, and light:dark. Physiology and Behavior, 53, 509–516. doi.org/10.1016/0031-9384(93)90145-6.
Partch, C. L., Green, C. B. & Takahashi, J. S. (2014). Molecular architecture of the mammalian circadian clock. Trends in Cell Biology, 24(2), 90-99. doi: 10.1016/j.tcb.2013.07.002.
Reddy, A. B., Karp, N. A., Maywood, E. S., Sage, E. A., Deery, M. & O’Neill, J. S. Circadian orchestration of the hepatic proteome. Current Biology, 16, 1107–1115. doi: 10.1016/j.cub.2006.04.026.
Renthlei, Z., Gurumayum, T., Borah, B. K. & Trivedi, A. K. (2019). Daily expression of clock genes in central and peripheral tissues of tree sparrow (Passer montanus). Chronobiology International, 36, 110–121. doi.org/10.108 0/07420528.2018.1523185.
Renthlei, Z. & Trivedi, A. K. (2019). Effect of urban environment on pineal machinery and clock genes expression of tree sparrow (Passer montanus). Environmental Pollution, 255(2), 113278. doi.org/10.1016/j.envpol.201 9.113278.
Sabath, E., Salgado-Delgado, R., Guerrero-Vargas, N. N., Guzman-Ruiz, M. A., Basualdo, M. C., Escobar, C. & Ruud, Buijs, R. M. (2014). Food entrains clock genes but not metabolic genes in the liver of suprachiasmatic nucleus lesioned rats. FEBS Letters, 588, 3104-3110. doi.org/10.1016/j.febslet.2014.06.045.
Sharma, V. K., Chidambaram, R. & Chandrashekaran, M. K. (2000). Probing the circadian pacemaker of a mouse using two light pulses. Journal of Biological Rhythms, 15, 67–73.
Stephan, F. K., Swann, J. M. & Sisk, C. L. (1979). Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. Behavioral and Neural Biology, 25, 346–363. doi.org/10.1016/S0163-1047(79)90415-1.
Stephan, F. K., Berkley, K. J. & Moss, R. L. (1981). Efferent connections of the rat suprachiasmatic nucleus. Neuroscience, 6, 2625–2641. doi: 10.1016/0306-4522(81)90108-1.
Stephan, F. K. (2001). Food entrainable oscillators in Mammals. In Takahashi J, Turek FW & Moore Y (eds). Handbook of behavioural Neurobiology 12: Circadian clocks. Plenum Publishers, New York, pp. 223-241. doi: 10.1007/978-1-4615-1201-1_9.
Stokkan, K. A., Yamazaki, S., Tei, H., Sakaki, Y. & Menaker, M. (2001). Entrainment of the circadian clock in the liver by feeding. Science, 291, 490-493. doi: 10.1126/science.291.5503.490.
Ventura, M. A., Gardey, C. & d’Athis, P. (1984). Rapid reset of the corticosterone rhythm by food presentation in rats under a circadian restricted feeding schedule. Chronobiology International, 1, 287–295. doi: 10.3109/074205 28409063909.
Vera, L. M., de Pedro, N., Gómez-Milán, E., Delgado, M. J., Sánchez-Muros, M. J., Madrid, J. A. & Sánchez-Vázquez, F. J. (2007). Feeding entrainment of locomotor activity rhythms, digestive enzymes and neuroendocrine factors in goldfish. Physiology and Behavior, 90, 518–524. doi.org/10.1016/j.physbeh.2006.10.017.
Wakamatsu, H., Yoishinobu, Y., Aida, R., Moriy, T., Akiyama, M. & Shibata, S. (2001). Restricted-feeding-induced anticipatory activity rhythm in associated with a phase-shift of the expression in mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nuc-leus of mice. European Journal of Neuroscience, 13, 1190–1196. doi: 10.1046/j.0953-816x.2001.014 83.x.
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M. & Tei, H. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science, 288, 682–685. doi: 10.1126/science.288.5466.682.
Yoo, S. H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H. K., Oh, W. J., Yoo, O. J., Menaker, M. & Takahashi, J. S. (2004). PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proceedings of the National Academy of Sciences, USA. 101, 5339–5346. doi: 10.1073/pnas.0308709101.
Balsalobre, A., Marcacc, L. & Schibler, U. (2000). Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Current Biology, 10, 1291–1294. https://doi.org/10.1016/S0960-9822(00)00758-2.
Borah, B. K., Renthlei, Z. & Trivedi, A. K. (2020). Hypothalamus but not liver retains daily expression of clock genes during hibernation in terai tree frog (Polypedates teraiensis). Chronobiology International, 37(4), 485–492. doi: 10.1080/07420528.2020.1726373.
Breno T. S. Carneiro, B. T. S., Fernandes, D. A. C., Medeiros, C. F. P., Diniz, N. L., Araujo, J. F. (2012). Daily anticipatory rhythms of behavior and body temperature in response to glucose availability in rats. Psychology & Neuroscience, 5(2), 191-197. doi.org/10.3922/j.psns.20 12.2.09.
Cassone, V. M. & Stephan, F. K. (2002). Central and peripheral regulation of feeding and nutrition by the mammalian circadian clock: implications for nutrition during manned space flight. Nutrition, 18(10), 814–819. doi.org/10.1016/S0899-9007(02)00937-1.
Challet, E., Caldelas, I., Graff, C. & Pevet, P. (2003). Synchronization of the molecular clockwork by light- and food-related cues in mammals. Biological Chemistry, 384, 711–719. doi: 10.1515/bc.2003.079. doi: 10.1515/BC.2003.079
Coleman, G. J., Harper, S., Clarke, J. D. & Armstrong, S. (1982). Evidence for a separate meal associated oscillator in the rat. Physiology and Behavior, 29, 107–115. https://doi.org/10.1016/0031-9384(82)90373-0.
Cox, K. H. & Takahashi, J. S. Circadian clock genes and the transcriptional architecture of the clock mechanism. Journal of Molecular Endocrinology, 63(4), R93-R102. doi: 10.1530/JME-19-0153. doi: 10.1530/JME-19-0153.
Cuesta, M., Clesse, D., Pe ́Vet, P. & Challet, E. (2009). From daily behaviour to hormonal and neurotransmitters rhythms: Comparison between diurnal and nocturnal rat species. Hormones and Behavior, 55, 338–347. doi.org/10.1016/j.yhbeh.2008.10.015.
Damiola, F., Le, Minh, 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, 2950–2961. doi: 10.1101/gad.183500.
Davidson, A. J., Aragona, B. J., Werner, R. M., Schroeder, E., Smith, J. C. & Stephan, F. K. Food anticipatory activity persists after olfactory bulb ablation in the rat. Physiology and Behavior, 72, 231–235. doi: 10.1016/s0031-9384(00)00417-0.
Dibner, C., Schibler, U. & Albrecht, U. (2010). The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annual Review of Physiology, 72, 517–549. doi: 10.1146/annurev-physiol-021909-135821.
Feillet, C. A., Mendoza, J., Pevet, P. & Challet, E. (2008). Restricted feeding restores rhythmicity in the pineal gland of arrhythmic suprachiasmatic-lesioned rats. European Journal of Neuroscience, 28, 2451–2458. doi: 10.1111/j.1460-9568.2008.06538.x.
Garaulet, M. & Gómez-Abellán, P. (2014). Timing of food intake and obesity: a novel association. Physiology and Behavior, 134, 44–50. doi: 10.1016/j.physbeh.20 14.0 1.001.
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, 269-278. doi: 10.1046/j.1365-2443.2001.00419.x.
Hernández-Pérez, J., Míguez, J. M., Naderi, F., Soengas, J. L. & López-Patiño, M. A. (2017). Influence of light and food on the circadian clock in liver of rainbow trout, Oncorhynchus mykiss. Chronobiology International, 34(9), 1259–1272. doi.org/10.1080/07420528.2017.1361435.
Honma, K., von Goetz, C. & Aschoff, J. (1983). Effects of restricted daily feeding on free running circadian rhythms in rats. Physiology and Behavior, 30, 905–913. doi.org/10.1016/0031-9384(83)90256-1.
Kamphuis, W., Cailotto, C., Dijk, F., Bergen, A. & Buijs, R. M. (2005). Circadian expression of clock genes and clock-controlled genesin the rat retina. Biochemical and Biophysical Research Communications, 330, 18–26. doi: 10.1016/j.bbrc.2005.02.118.
Kornmann, B., Preitner, N., Rifat, D., Fleury-Olela, F. & Schibler, U. (2001). Analysis of circadian liver gene expression by ADDER, a highly sensitive method for the display of differentially expressed mRNAs. Nucleic Acids Research, 29, E51– 51. doi: 10.1093/nar/29.11.e51.
Krizo,J. A., Moreland, L. E., Rastogi, A., Mou, X., Prosser, R. A., Mintz, E. A. (2018). Regulation of Locomotor activity in fed, fasted, and food-restricted mice lacking tissue-type plasminogen activator. BMC Physiology,18:2. doi: 10.1186/s12899-018-0036-0.
Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(–ddC(T)) method. Methods, 25, 402–408. doi: 10.1006/meth.2001.1262.
McHill, A. W., Phillips, A. J., Czeisler, C. A., Keating, L., Yee, K., Barger, L. K., Garaulet, M., Scheer, F. A. & Klerman, E. B. (2017). Later circadian timing of food intake is associated with increased body fat. American Journal of Clinical Nutrition, 106(5), 1213–1219. doi.org/10.3945/ajcn.117.161588.
Mendez, M. A., Popkin, B. M., Buckland, G., Schroder, H., Amiano, P., Barricarte, A., Huert, J. M., Quirós, R. J., Sánchez, M. J. & González, C. A. (2011). Alternative methods of accounting for underreporting and overreporting when measuring dietary intake–obesity relations. American Journal of Epidemiology, 173, 448–58. doi: 10.1093/aje/kwq380.
Mistlberger, R. E. (1994). Circadian food-anticipatory activity: formal models and physiological mechanisms. Neuroscience and Biobehavioral Reviews, 18, 171–195. doi.org/10.1016/0149-7634(94)90023-X.
Mistlberger, R. E. (1993). Effects of scheduled food and water access on circadian rhythms of hamsters in constant light, dark, and light:dark. Physiology and Behavior, 53, 509–516. doi.org/10.1016/0031-9384(93)90145-6.
Partch, C. L., Green, C. B. & Takahashi, J. S. (2014). Molecular architecture of the mammalian circadian clock. Trends in Cell Biology, 24(2), 90-99. doi: 10.1016/j.tcb.2013.07.002.
Reddy, A. B., Karp, N. A., Maywood, E. S., Sage, E. A., Deery, M. & O’Neill, J. S. Circadian orchestration of the hepatic proteome. Current Biology, 16, 1107–1115. doi: 10.1016/j.cub.2006.04.026.
Renthlei, Z., Gurumayum, T., Borah, B. K. & Trivedi, A. K. (2019). Daily expression of clock genes in central and peripheral tissues of tree sparrow (Passer montanus). Chronobiology International, 36, 110–121. doi.org/10.108 0/07420528.2018.1523185.
Renthlei, Z. & Trivedi, A. K. (2019). Effect of urban environment on pineal machinery and clock genes expression of tree sparrow (Passer montanus). Environmental Pollution, 255(2), 113278. doi.org/10.1016/j.envpol.201 9.113278.
Sabath, E., Salgado-Delgado, R., Guerrero-Vargas, N. N., Guzman-Ruiz, M. A., Basualdo, M. C., Escobar, C. & Ruud, Buijs, R. M. (2014). Food entrains clock genes but not metabolic genes in the liver of suprachiasmatic nucleus lesioned rats. FEBS Letters, 588, 3104-3110. doi.org/10.1016/j.febslet.2014.06.045.
Sharma, V. K., Chidambaram, R. & Chandrashekaran, M. K. (2000). Probing the circadian pacemaker of a mouse using two light pulses. Journal of Biological Rhythms, 15, 67–73.
Stephan, F. K., Swann, J. M. & Sisk, C. L. (1979). Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. Behavioral and Neural Biology, 25, 346–363. doi.org/10.1016/S0163-1047(79)90415-1.
Stephan, F. K., Berkley, K. J. & Moss, R. L. (1981). Efferent connections of the rat suprachiasmatic nucleus. Neuroscience, 6, 2625–2641. doi: 10.1016/0306-4522(81)90108-1.
Stephan, F. K. (2001). Food entrainable oscillators in Mammals. In Takahashi J, Turek FW & Moore Y (eds). Handbook of behavioural Neurobiology 12: Circadian clocks. Plenum Publishers, New York, pp. 223-241. doi: 10.1007/978-1-4615-1201-1_9.
Stokkan, K. A., Yamazaki, S., Tei, H., Sakaki, Y. & Menaker, M. (2001). Entrainment of the circadian clock in the liver by feeding. Science, 291, 490-493. doi: 10.1126/science.291.5503.490.
Ventura, M. A., Gardey, C. & d’Athis, P. (1984). Rapid reset of the corticosterone rhythm by food presentation in rats under a circadian restricted feeding schedule. Chronobiology International, 1, 287–295. doi: 10.3109/074205 28409063909.
Vera, L. M., de Pedro, N., Gómez-Milán, E., Delgado, M. J., Sánchez-Muros, M. J., Madrid, J. A. & Sánchez-Vázquez, F. J. (2007). Feeding entrainment of locomotor activity rhythms, digestive enzymes and neuroendocrine factors in goldfish. Physiology and Behavior, 90, 518–524. doi.org/10.1016/j.physbeh.2006.10.017.
Wakamatsu, H., Yoishinobu, Y., Aida, R., Moriy, T., Akiyama, M. & Shibata, S. (2001). Restricted-feeding-induced anticipatory activity rhythm in associated with a phase-shift of the expression in mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nuc-leus of mice. European Journal of Neuroscience, 13, 1190–1196. doi: 10.1046/j.0953-816x.2001.014 83.x.
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M. & Tei, H. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science, 288, 682–685. doi: 10.1126/science.288.5466.682.
Yoo, S. H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H. K., Oh, W. J., Yoo, O. J., Menaker, M. & Takahashi, J. S. (2004). PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proceedings of the National Academy of Sciences, USA. 101, 5339–5346. doi: 10.1073/pnas.0308709101.
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How to Cite
Food, not the photoperiod, entrains the circadian rhythms in the liver of Winstar albino rats. (2022). Journal of Applied and Natural Science, 14(2), 559-565. https://doi.org/10.31018/jans.v14i2.3447
