Effect of photoperiodic alterations and binge eating on biochemical and metabolic parameters in zebrafish (Danio rerio)
Article Main
Abstract
Altered sleep-wake cycles and irregular eating patterns are among the most prominent lifestyle changes observed due to the increasing trend of shift work worldwide. Though circadian rhythm disruptions and unhealthy eating practices are increasingly recognized as contributors to metabolic disorders in humans, the underlying mechanisms remain unclear. The present study investigated the combined effects of binge eating and altered photoperiods on the metabolic and biochemical profiles of zebrafish (Danio rerio), a well-established vertebrate model. Adult zebrafish were subjected to excessive feeding and altered photoperiod (20 h light: 4 h dark) for two weeks, while the age-matched control group were maintained in standard laboratory conditions. Important biochemical indicators, such as blood glucose, nitric oxide, and the activities of the antioxidant enzymes superoxide dismutase (SOD) and catalase (CAT), were measured in addition to total protein. The present results showed that the blood glucose levels in the experimental group were significantly higher compared to the control group (76.2 ± 1.13 mg/dL vs. 52.9 ± 1.27 mg/dL). The antioxidant enzyme superoxide dismutase activity was significantly higher in the experimental group (56.02 ± 2.14 U/mg) compared to controls (3.18 ± 0.18 U/mg). The enzyme catalase also showed a slight but significant increase in its activity in the experimental group. However, Nitric oxide levels and total protein levels did not significantly change. These results showed that altering photoperiod in conjunction with altered feeding can lead to elevated glucose levels and increased oxidative stress, thereby affecting zebrafish metabolic homeostasis. This work provides a basic framework to understand the intricate relationship between circadian disruption and dietary excess in metabolic dysregulation, potentially impacting overall health.
Article Details
Article Details
Keywords
Binge eating, Circadian disruption, Homeostasis, Metabolism, Oxidative stress, Photoperiodic alterations, Zebrafish
References
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Bass, J., & Takahashi, J. S. (2010). Circadian integration of metabolism and energetics. Science, 330(6009), 1349-1354. DOI: https://doi.org/10.1126/science.1195027
Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1), 276–287. DOI: https://doi.org/10.1016/0003-2697(71)90370-8
Beaumont, M., Mordret, A., Gaggini, M., Weill, G., Coudé, M., Kessler, L., & Vinoy, S. (2023). Exploring the relationship between social jetlag with gut microbial composition, diet and cardiometabolic health, in the Zoe Predict 1 cohort. European Journal of Nutrition, 62(6), 2419-2437. DOI: https://doi.org/10.1007/s00394-023-03204-x
Boivin, D.B., Boudreau, P. and Kosmadopoulos, A. (2022). Disturbance of the circadian system in shift work and its health impact. Journal of biological rhythms, 37(1), 3-28. DOI: https://doi.org/10.1177/07487304211064218
CPCSEA (2021). Guidelines of the Committee for the purpose of control and supervision of experiments on animals CPCSEA for experimentation on fishes, Ministry of Fisheries, Animal Husbandry and Dairying, Department of Animal Husbandry and Dairying, Government of India. Link: https://ccsea.gov.in/Content/54_1_Acts,rulesand guideli nes.aspx
Demir, I., Toker, A., Aksoy, H., Tasyurek, E. & Zengin, S. (2021). The Impact of Shift Type on Oxidative Stress, Inflammation, and Platelet Activation. Journal of Occupational and Environmental Medicine, 63(3), e127-e131. DOI: https://doi.org/10.1097/JOM.0000000000002124
Dial, M.B., Malek, E.M., Cooper, A.R., Neblina, G.A., Vasileva, N.I. & McGinnis, G.R. (2025). Social jetlag alters markers of exercise-induced mitochondrial adaptations in the heart. npj Biological Timing and Sleep, 2(1), 4. DOI: https://doi.org/10.1038/s44323-024-00019-9
Fagiani, F., Di Marino, D., Romagnoli, A., Travelli, C., Voltan, D., Di Cesare Mannelli, L., Racchi, M., Govoni, S. & Lanni, C. (2022). Molecular regulations of circadian rhythm and implications for physiology and diseases. Signal transduction and targeted therapy, 7(1), 41. DOI: https://doi.org/10.1038/s41392-022-00899-y
Gardner, P., & McQUILLIN, J. (1980). Immunofluorescence techniques, control of specificity and non-specific fluorescence. Elsevier eBooks, 56–91. DOI: https://doi.org/10.1016/b978-0-407-38441-5.50010-x
Hatori, M., Vollmers, C., Zarrinpar, A., DiTacchio, L., Bushong, E. A., Gill, S., & Panda, S. (2012). Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metabolism, 15(6), 848-860. DOI: https://doi.org/10.1016/j.cmet.2012.04.019
Jin, Y., Shu, L., Sun, L., Liu, W., & Fu, Z. (2009). Temperature and photoperiod affect the endocrine disruption effects of ethinylestradiol, nonylphenol and their binary mixture in zebrafish (Danio rerio). Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology, 151(2), 258–263. DOI: https://doi.org/10.1016/j.cbpc.2009.11.004
Karlsson, B., Knutsson, A. & Lindahl, B. (2001). Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27 485 people. Occupational and environmental medicine, 58(11), 747-752. DOI: https://doi.org/10.1136/oem.58.11.747
Khapre, R. V., Kondratova, A. A., Susova, O., & Kondratov, R. V. (2011). Circadian clock protein BMAL1 regulates cellular senescence in vivo. Cell Cycle, 10(23), 4162-4169. DOI: https://doi.org/10.4161/cc.10.23.18381
Kyung, M., Park, S., Park, C.G. & Hong, O. (2024). Association between sleep duration, social jetlag, and the metabolic syndrome by shift works. International Journal of Environmental Research and Public Health, 21(6), 668. DOI: https://doi.org/10.3390/ijerph21060668
Knutsson, A., & Kempe, A. (2014). Shift work and diabetes–a systematic review. Chronobiology International, 31(10), 1146-1151. DOI: https://doi.org/10.310 9/07420528.2014.957308
López‐Olmeda, J. F., Madrid, J. A., & Sánchez‐Vázquez, F. J. (2006). Light and Temperature Cycles as Zeitgebers of Zebrafish (Danio rerio) Circadian Activity Rhythms. Chronobiology International, 23(3), 537–550. DOI: https://doi.org/10.1080/07420520600651065
López-Olmeda, J. F., & Sánchez-Vázquez, F. J. (2011). Thermal biology of zebrafish (Danio rerio). Journal of Thermal Biology, 36(2), 91-104. DOI: https://doi.org/10.1016/j.jtherbio.2010.12.005
Lucon-Xiccato, T., Montalbano, G., Frigato, E., Loosli, F., Foulkes, N. S., & Bertolucci, C. (2022). Medaka as a model for seasonal plasticity: Photoperiod-mediated changes in behaviour, cognition, and hormones. Hormones and Behavior, 145, 105244. DOI: https://doi.org/10.1016/j.yhbeh.2022.105244
Mason, I. C., Qian, J., Adler, G. K., & Scheer, F. A. (2020). Impact of circadian disruption on glucose metabolism: implications for type 2 diabetes. Diabetologia, 63(3), 462-472. DOI: https://doi.org/10.1007/s00125-019-050
59-6
Mæhre, H., Jensen, I., & Eilertsen, K. (2016). Enzymatic Pre-Treatment Increases the Protein Bioaccessibility and Extractability in Dulse (Palmaria palmata). Marine Drugs, 14(11), 196. DOI: https://doi.org/10.3390/md14110196
Morbiato, E., Frigato, E., Dinarello, A., Maradonna, F., Facchinello, N., Argenton, F., Carnevali, O., Valle, L. D., & Bertolucci, C. (2019). Feeding entrainment of the zebrafish circadian clock is regulated by the glucocorticoid receptor. Cells, 8(11): 1342. DOI: https://doi.org/10.3390/cells8111342
Hadwan, M. H., Hussein, M. J., Mohammed, R. M., Hadwan, A. M., Saad Al-Kawaz, H., Al-Obaidy, S. S., & Al Talebi, Z. A. (2024). An improved method for measuring catalase activity in biological samples. Biology Methods and Protocols, 9(1) bpae015. DOI: https://doi.org/10.1093/biomethods/bpae015
Morris, C. J., Yang, J. N., Garcia, J. I., Myers, S., Bozzi, I., Wang, W., & Scheer, F. A. (2015). Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans. Proceedings of the National Academy of Sciences, 112(17), E2225-E2234. DOI: https://doi.org/10.1073/pnas.1418955112
Teixeira, K.R., Dos Santos, C.P., de Medeiros, L.A., Mendes, J.A., Cunha, T.M., De Angelis, K., Penha-Silva, N., de Oliveira, E.P. & Crispim, C.A. (2019). Night workers have lower levels of antioxidant defenses and higher levels of oxidative stress damage when compared to day workers. Scientific reports, 9(1), 4455. DOI: https://doi.org/10.1038/s41598-019-40989-6
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: https://doi.org/10.1016/j.tcb.2013.07.002
Pedroso, G. L., Hammes, T. O., Escobar, T. D., Fracasso, L. B., Forgiarini, L. F., & Da Silveira, T. R. (2012). Blood collection for biochemical analysis in adult zebrafish. Journal of Visualized Experiments, (63), e3865. DOI: https://doi.org/10.3791/3865
Peterson, G.L. (1977). A simplification of the protein assay method of Lowry et al. which is more generally applicable. Analytical biochemistry, 83(2), 346-356. DOI: https://doi.org/10.1016/0003-2697(77)90043-4
Potter, G. D., Skene, D. J., Arendt, J., Cade, J. E., Grant, P. J., & Hardie, L. J. (2016). Circadian rhythm and sleep disruption: causes, metabolic consequences, and countermeasures. Endocrine Reviews, 37(6), 584-608. DOI: https://doi.org/10.1210/er.2016-1083
Reid, K. J., Santostasi, G., Baron, K. G., Wilson, J., Kang, J., & Zee, P. C. (2014). Timing and intensity of light correlate with body weight in adults. PLoS One, 9(4), e92251. DOI: https://doi.org/10.1371/journal.pone.0092251
Reiter, R. J., Rosales-Corral, S., Coto-Montes, A., Antonio Boga, J., Tan, D. X., Davis, J. M., Konturek, P. C., Konturek, S. J. & Brzozowski, T. (2011). The photoperiod, circadian regulation and chronodisruption: the requisite interplay between the suprachiasmatic nuclei and the pineal and gut melatonin. Journal of Physiology and Pharmacology, 62(3), 269-274. Link: https://pubme d.ncbi.nlm.nih.gov/21893686/
Scheer, F. A., Hilton, M. F., Mantzoros, C. S., & Shea, S. A. (2009). Adverse metabolic and cardiovascular consequences of circadian misalignment. Proceedings of the National Academy of Sciences, 106(11), 4453-4458. DOI: https://doi.org/10.1073/pnas.0808180106
Schettini, M.A.S., do Nascimento Passos, R.F. & Koike, B.D.V. (2023). Shift work and metabolic syndrome updates: a systematic review. Sleep Science, 16(02), 237-247. DOI: https://doi.org/10.1055/s-0043-1770798
Sorokin, I. E., Evsyukova, V. S., & Kulikov, A. V. (2022). Effect of Short Photoperiod on the Behavior and Brain Serotonin System in Zebrafish Danio rerio. Bulletin of Experimental Biology and Medicine, 173(3), 293–297. DOI: https://doi.org/10.1007/s10517-022-05536-w
Takahashi, J. S. (2017). Transcriptional architecture of the mammalian circadian clock. Nature Reviews Genetics, 18(3), 164-179. DOI: https://doi.org/10.1038/nrg.2016.150
Thraya, M., Patel, A., Stewart, K., Abou-Akl, H., Roberts, D., Heath, D., Pitcher, T.E., Carmona-Alcocer, V. & Karpowicz, P. (2025). Integration of photoperiod and time-restricted feeding on the circadian gene rhythms in juvenile salmon. Scientific Reports, 15(1), 16156. DOI: https://doi.org/10.1038/s41598-025-01069-0
Villamizar, N., Vera, L. M., Foulkes, N. S., & Sánchez-Vázquez, F. J. (2014). Effect of lighting conditions on zebrafish growth and development. Zebrafish, 11(2), 173-181. DOI: https://doi.org/10.1089/zeb.2013.0926
Whitmore, D., Foulkes, N. S., & Sassone-Corsi, P. (2000). Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature, 404(6773), 87-91. DOI: https://doi.org/10.1038/35003589
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., & Tei, H. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science, 288(5466), 682-685. DOI: https://doi.org/10.1126/science.288.5466.682
Yucel, A., Gulen, S., Dincer, S., Yucel, A., & Yetkin, G. (2012). Comparison of two different applications of the Griess method for nitric oxide measurement. Journal of Experimental and Integrative Medicine, 2(2), 167. DOI: https://doi.org/10.5455/jeim.200312.or.024
Zhao, M., Wan, J., Zeng, K., Tong, M., Lee, A. C., Ding, J., & Chen, Q. (2016). The reduction in circulating melatonin level may contribute to the pathogenesis of ovarian cancer: a retrospective study. Journal of Cancer, 9(5), 831-839. DOI: https://doi.org/10.7150/jca.14573
Zimmet, P., Alberti, K. G. M., Stern, N., Bilu, C., El-Osta, A., Einat, H., & Kronfeld-Schor, N. (2019). The circadian syndrome: is the metabolic syndrome and much more! Journal of Internal Medicine, 286(2), 181-191. DOI: https://doi.org/10.1111/joim.12924
Zou, Y., Ma, X., Chen, Q., Xu, E., Yu, J., Tang, Y., Wang, D., Yu, S. & Qiu, L. (2023). Nightshift work can induce oxidative DNA damage: a pilot study. BMC Public Health, 23(1), 891. DOI: https://doi.org/10.1186/s12889-023-15742-4
Bass, J., & Takahashi, J. S. (2010). Circadian integration of metabolism and energetics. Science, 330(6009), 1349-1354. DOI: https://doi.org/10.1126/science.1195027
Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1), 276–287. DOI: https://doi.org/10.1016/0003-2697(71)90370-8
Beaumont, M., Mordret, A., Gaggini, M., Weill, G., Coudé, M., Kessler, L., & Vinoy, S. (2023). Exploring the relationship between social jetlag with gut microbial composition, diet and cardiometabolic health, in the Zoe Predict 1 cohort. European Journal of Nutrition, 62(6), 2419-2437. DOI: https://doi.org/10.1007/s00394-023-03204-x
Boivin, D.B., Boudreau, P. and Kosmadopoulos, A. (2022). Disturbance of the circadian system in shift work and its health impact. Journal of biological rhythms, 37(1), 3-28. DOI: https://doi.org/10.1177/07487304211064218
CPCSEA (2021). Guidelines of the Committee for the purpose of control and supervision of experiments on animals CPCSEA for experimentation on fishes, Ministry of Fisheries, Animal Husbandry and Dairying, Department of Animal Husbandry and Dairying, Government of India. Link: https://ccsea.gov.in/Content/54_1_Acts,rulesand guideli nes.aspx
Demir, I., Toker, A., Aksoy, H., Tasyurek, E. & Zengin, S. (2021). The Impact of Shift Type on Oxidative Stress, Inflammation, and Platelet Activation. Journal of Occupational and Environmental Medicine, 63(3), e127-e131. DOI: https://doi.org/10.1097/JOM.0000000000002124
Dial, M.B., Malek, E.M., Cooper, A.R., Neblina, G.A., Vasileva, N.I. & McGinnis, G.R. (2025). Social jetlag alters markers of exercise-induced mitochondrial adaptations in the heart. npj Biological Timing and Sleep, 2(1), 4. DOI: https://doi.org/10.1038/s44323-024-00019-9
Fagiani, F., Di Marino, D., Romagnoli, A., Travelli, C., Voltan, D., Di Cesare Mannelli, L., Racchi, M., Govoni, S. & Lanni, C. (2022). Molecular regulations of circadian rhythm and implications for physiology and diseases. Signal transduction and targeted therapy, 7(1), 41. DOI: https://doi.org/10.1038/s41392-022-00899-y
Gardner, P., & McQUILLIN, J. (1980). Immunofluorescence techniques, control of specificity and non-specific fluorescence. Elsevier eBooks, 56–91. DOI: https://doi.org/10.1016/b978-0-407-38441-5.50010-x
Hatori, M., Vollmers, C., Zarrinpar, A., DiTacchio, L., Bushong, E. A., Gill, S., & Panda, S. (2012). Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metabolism, 15(6), 848-860. DOI: https://doi.org/10.1016/j.cmet.2012.04.019
Jin, Y., Shu, L., Sun, L., Liu, W., & Fu, Z. (2009). Temperature and photoperiod affect the endocrine disruption effects of ethinylestradiol, nonylphenol and their binary mixture in zebrafish (Danio rerio). Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology, 151(2), 258–263. DOI: https://doi.org/10.1016/j.cbpc.2009.11.004
Karlsson, B., Knutsson, A. & Lindahl, B. (2001). Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27 485 people. Occupational and environmental medicine, 58(11), 747-752. DOI: https://doi.org/10.1136/oem.58.11.747
Khapre, R. V., Kondratova, A. A., Susova, O., & Kondratov, R. V. (2011). Circadian clock protein BMAL1 regulates cellular senescence in vivo. Cell Cycle, 10(23), 4162-4169. DOI: https://doi.org/10.4161/cc.10.23.18381
Kyung, M., Park, S., Park, C.G. & Hong, O. (2024). Association between sleep duration, social jetlag, and the metabolic syndrome by shift works. International Journal of Environmental Research and Public Health, 21(6), 668. DOI: https://doi.org/10.3390/ijerph21060668
Knutsson, A., & Kempe, A. (2014). Shift work and diabetes–a systematic review. Chronobiology International, 31(10), 1146-1151. DOI: https://doi.org/10.310 9/07420528.2014.957308
López‐Olmeda, J. F., Madrid, J. A., & Sánchez‐Vázquez, F. J. (2006). Light and Temperature Cycles as Zeitgebers of Zebrafish (Danio rerio) Circadian Activity Rhythms. Chronobiology International, 23(3), 537–550. DOI: https://doi.org/10.1080/07420520600651065
López-Olmeda, J. F., & Sánchez-Vázquez, F. J. (2011). Thermal biology of zebrafish (Danio rerio). Journal of Thermal Biology, 36(2), 91-104. DOI: https://doi.org/10.1016/j.jtherbio.2010.12.005
Lucon-Xiccato, T., Montalbano, G., Frigato, E., Loosli, F., Foulkes, N. S., & Bertolucci, C. (2022). Medaka as a model for seasonal plasticity: Photoperiod-mediated changes in behaviour, cognition, and hormones. Hormones and Behavior, 145, 105244. DOI: https://doi.org/10.1016/j.yhbeh.2022.105244
Mason, I. C., Qian, J., Adler, G. K., & Scheer, F. A. (2020). Impact of circadian disruption on glucose metabolism: implications for type 2 diabetes. Diabetologia, 63(3), 462-472. DOI: https://doi.org/10.1007/s00125-019-050
59-6
Mæhre, H., Jensen, I., & Eilertsen, K. (2016). Enzymatic Pre-Treatment Increases the Protein Bioaccessibility and Extractability in Dulse (Palmaria palmata). Marine Drugs, 14(11), 196. DOI: https://doi.org/10.3390/md14110196
Morbiato, E., Frigato, E., Dinarello, A., Maradonna, F., Facchinello, N., Argenton, F., Carnevali, O., Valle, L. D., & Bertolucci, C. (2019). Feeding entrainment of the zebrafish circadian clock is regulated by the glucocorticoid receptor. Cells, 8(11): 1342. DOI: https://doi.org/10.3390/cells8111342
Hadwan, M. H., Hussein, M. J., Mohammed, R. M., Hadwan, A. M., Saad Al-Kawaz, H., Al-Obaidy, S. S., & Al Talebi, Z. A. (2024). An improved method for measuring catalase activity in biological samples. Biology Methods and Protocols, 9(1) bpae015. DOI: https://doi.org/10.1093/biomethods/bpae015
Morris, C. J., Yang, J. N., Garcia, J. I., Myers, S., Bozzi, I., Wang, W., & Scheer, F. A. (2015). Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans. Proceedings of the National Academy of Sciences, 112(17), E2225-E2234. DOI: https://doi.org/10.1073/pnas.1418955112
Teixeira, K.R., Dos Santos, C.P., de Medeiros, L.A., Mendes, J.A., Cunha, T.M., De Angelis, K., Penha-Silva, N., de Oliveira, E.P. & Crispim, C.A. (2019). Night workers have lower levels of antioxidant defenses and higher levels of oxidative stress damage when compared to day workers. Scientific reports, 9(1), 4455. DOI: https://doi.org/10.1038/s41598-019-40989-6
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: https://doi.org/10.1016/j.tcb.2013.07.002
Pedroso, G. L., Hammes, T. O., Escobar, T. D., Fracasso, L. B., Forgiarini, L. F., & Da Silveira, T. R. (2012). Blood collection for biochemical analysis in adult zebrafish. Journal of Visualized Experiments, (63), e3865. DOI: https://doi.org/10.3791/3865
Peterson, G.L. (1977). A simplification of the protein assay method of Lowry et al. which is more generally applicable. Analytical biochemistry, 83(2), 346-356. DOI: https://doi.org/10.1016/0003-2697(77)90043-4
Potter, G. D., Skene, D. J., Arendt, J., Cade, J. E., Grant, P. J., & Hardie, L. J. (2016). Circadian rhythm and sleep disruption: causes, metabolic consequences, and countermeasures. Endocrine Reviews, 37(6), 584-608. DOI: https://doi.org/10.1210/er.2016-1083
Reid, K. J., Santostasi, G., Baron, K. G., Wilson, J., Kang, J., & Zee, P. C. (2014). Timing and intensity of light correlate with body weight in adults. PLoS One, 9(4), e92251. DOI: https://doi.org/10.1371/journal.pone.0092251
Reiter, R. J., Rosales-Corral, S., Coto-Montes, A., Antonio Boga, J., Tan, D. X., Davis, J. M., Konturek, P. C., Konturek, S. J. & Brzozowski, T. (2011). The photoperiod, circadian regulation and chronodisruption: the requisite interplay between the suprachiasmatic nuclei and the pineal and gut melatonin. Journal of Physiology and Pharmacology, 62(3), 269-274. Link: https://pubme d.ncbi.nlm.nih.gov/21893686/
Scheer, F. A., Hilton, M. F., Mantzoros, C. S., & Shea, S. A. (2009). Adverse metabolic and cardiovascular consequences of circadian misalignment. Proceedings of the National Academy of Sciences, 106(11), 4453-4458. DOI: https://doi.org/10.1073/pnas.0808180106
Schettini, M.A.S., do Nascimento Passos, R.F. & Koike, B.D.V. (2023). Shift work and metabolic syndrome updates: a systematic review. Sleep Science, 16(02), 237-247. DOI: https://doi.org/10.1055/s-0043-1770798
Sorokin, I. E., Evsyukova, V. S., & Kulikov, A. V. (2022). Effect of Short Photoperiod on the Behavior and Brain Serotonin System in Zebrafish Danio rerio. Bulletin of Experimental Biology and Medicine, 173(3), 293–297. DOI: https://doi.org/10.1007/s10517-022-05536-w
Takahashi, J. S. (2017). Transcriptional architecture of the mammalian circadian clock. Nature Reviews Genetics, 18(3), 164-179. DOI: https://doi.org/10.1038/nrg.2016.150
Thraya, M., Patel, A., Stewart, K., Abou-Akl, H., Roberts, D., Heath, D., Pitcher, T.E., Carmona-Alcocer, V. & Karpowicz, P. (2025). Integration of photoperiod and time-restricted feeding on the circadian gene rhythms in juvenile salmon. Scientific Reports, 15(1), 16156. DOI: https://doi.org/10.1038/s41598-025-01069-0
Villamizar, N., Vera, L. M., Foulkes, N. S., & Sánchez-Vázquez, F. J. (2014). Effect of lighting conditions on zebrafish growth and development. Zebrafish, 11(2), 173-181. DOI: https://doi.org/10.1089/zeb.2013.0926
Whitmore, D., Foulkes, N. S., & Sassone-Corsi, P. (2000). Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature, 404(6773), 87-91. DOI: https://doi.org/10.1038/35003589
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., & Tei, H. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science, 288(5466), 682-685. DOI: https://doi.org/10.1126/science.288.5466.682
Yucel, A., Gulen, S., Dincer, S., Yucel, A., & Yetkin, G. (2012). Comparison of two different applications of the Griess method for nitric oxide measurement. Journal of Experimental and Integrative Medicine, 2(2), 167. DOI: https://doi.org/10.5455/jeim.200312.or.024
Zhao, M., Wan, J., Zeng, K., Tong, M., Lee, A. C., Ding, J., & Chen, Q. (2016). The reduction in circulating melatonin level may contribute to the pathogenesis of ovarian cancer: a retrospective study. Journal of Cancer, 9(5), 831-839. DOI: https://doi.org/10.7150/jca.14573
Zimmet, P., Alberti, K. G. M., Stern, N., Bilu, C., El-Osta, A., Einat, H., & Kronfeld-Schor, N. (2019). The circadian syndrome: is the metabolic syndrome and much more! Journal of Internal Medicine, 286(2), 181-191. DOI: https://doi.org/10.1111/joim.12924
Zou, Y., Ma, X., Chen, Q., Xu, E., Yu, J., Tang, Y., Wang, D., Yu, S. & Qiu, L. (2023). Nightshift work can induce oxidative DNA damage: a pilot study. BMC Public Health, 23(1), 891. DOI: https://doi.org/10.1186/s12889-023-15742-4
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Effect of photoperiodic alterations and binge eating on biochemical and metabolic parameters in zebrafish (Danio rerio). (2025). Journal of Applied and Natural Science, 17(3), 1299-1305. https://doi.org/10.31018/jans.v17i3.6748
