Influences of Breakfast on Clock Gene Expression and Postprandial Glycemia in Healthy Individuals and Individuals With Diabetes: A Randomized Clinical Trial
Abstract
OBJECTIVE The circadian clock regulates glucose metabolism by mediating the activity of metabolic enzymes, hormones, and transport systems. Breakfast skipping and night eating have been associated with high HbA1c and postprandial hyperglycemia after lunch and dinner. Our aim was to explore the acute effect of breakfast consumption or omission on glucose homeostasis and clock gene expression in healthy individuals and individuals with type 2 diabetes. RESEARCH DESIGN AND METHODS In a crossover design, 18 healthy volunteers and 18 volunteers with 14.5 ± 1.5 years diabetes, BMI 30.7 ± 1.1 kg/m2, and HbA1c 7.6 ± 0.1% (59.6 ± 0.8 mmol/mol) were randomly assigned to a test day with breakfast and lunch (YesB) and a test day with only lunch (NoB). Postprandial clock and clock-controlled gene expression, plasma glucose, insulin, intact glucagon-like peptide 1 (iGLP-1), and dipeptidyl peptidase IV (DPP-IV) plasma activity were assessed after breakfast and lunch. RESULTS In healthy individuals, the expression level of Per1, Cry1, Rorα, and Sirt1 was lower (P < 0.05) but Clock was higher (P < 0.05) after breakfast. In contrast, in individuals with type 2 diabetes, Per1, Per2, and Sirt1 only slightly, but significantly, decreased and Rorα increased (P < 0.05) after breakfast. In healthy individuals, the expression level of Bmal1, Rorα, and Sirt1 was higher (P < 0.05) after lunch on YesB day, whereas the other clock genes remained unchanged. In individuals with type 2 diabetes, Bmal1, Per1, Per2, Rev-erbα, and Ampk increased (P < 0.05) after lunch on the YesB day. Omission of breakfast altered clock and metabolic gene expression in both healthy and individuals with type 2 diabetes. CONCLUSIONS Breakfast consumption acutely affects clock and clock-controlled gene expression leading to normal oscillation. Breakfast skipping adversely affects clock and clock-controlled gene expression and is correlated with increased postprandial glycemic response in both healthy individuals and individuals with diabetes.
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The effects of fasting until 12:00 on postprandial hyperglycemia and insulin responses are due to effects directly on clock genes and time-controlled genetic expression.
“due to effects directly on clock genes and time-controlled genetic expression [285].”
From Effects of diet, lifestyle, Chrononutrition and alternative dietary interventions on postprandial Glycemia and insulin resistance (2022) · cites this paper as [285]
Cites
AMPK: a nutrient and energy sensor that maintains energy homeostasis
Hardie, D. G., Ross, F. A., & Hawley, S. A. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3311 · Cited by 4,602 · see citing works
Coordination of circadian timing in mammals
Reppert, S. M., & Weaver, D. R. (2002) · Nature · doi:10.1038/nature00965 · Cited by 4,379 · see citing works
Adverse metabolic and cardiovascular consequences of circadian misalignment
Scheer, F. A. J. L., Hilton, M. F., Mantzoros, C. S., & Shea, S. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808180106 · Cited by 2,351 · see citing works
Preitner, N., Damiola, F., Luis-Lopez-Molina, Zakany, J., Duboule, D., Albrecht, U., & Schibler, U. (2002) · Cell · doi:10.1016/s0092-8674(02)00825-5 · Cited by 2,198 · see citing works
Hatori, M., Vollmers, C., Zarrinpar, A., DiTacchio, L., Bushong, E. A., Gill, S., Leblanc, M., Chaix, A., Joens, M., Fitzpatrick, J. A. J., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.04.019 · Cited by 1,986 · see citing works
SIRT1 regulates circadian clock gene expression through PER2 deacetylation
Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F. W., & Schibler, U. (2008) · Cell · doi:10.1016/j.cell.2008.06.050 · Cited by 1,376 · see citing works
Circadian Control of the NAD <sup>+</sup> Salvage Pathway by CLOCK-SIRT1
Nakahata, Y., Sahar, S., Astarita, G., Kaluzova, M., & Sassone-Corsi, P. (2009) · Science · doi:10.1126/science.1170803 · Cited by 1,198 · see citing works
A Functional Genomics Strategy Reveals Rora as a Component of the Mammalian Circadian Clock
Sato, T. K., Panda, S., Miraglia, L. J., Reyes, T. M., Rudic, R. D., McNamara, P., Naik, K. A., FitzGerald, G. A., Kay, S. A., & Hogenesch, J. B. (2004) · Neuron · doi:10.1016/j.neuron.2004.07.018 · Cited by 1,115 · see citing works
AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation
Lamia, K. A., Sachdeva, U. M., DiTacchio, L., Williams, E. C., Alvarez, J. G., Egan, D. F., Vasquez, D. S., Juguilon, H., Panda, S., Shaw, R. J., et al. (2009) · Science · doi:10.1126/science.1172156 · Cited by 958 · see citing works
Chaix, A., Zarrinpar, A., Miu, P., & Panda, S. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.11.001 · Cited by 956 · see citing works
Circadian timing of food intake contributes to weight gain
Arble, D. M., Bass, J., Laposky, A. D., Vitaterna, M. H., & Turek, F. W. (2009) · Obesity · doi:10.1038/oby.2009.264 · Cited by 953 · see citing works
A transcription factor response element for gene expression during circadian night
Ueda, H. R., Chen, W., Adachi, A. A., Wakamatsu, H., Hayashi, S., Takasugi, T., Nagano, M., Nakahama, K., Suzuki, Y., Sugano, S., et al. (2002) · Nature · doi:10.1038/nature00906 · Cited by 850 · see citing works
Metabolism and Circadian Rhythms—Implications for Obesity
Froy, O. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0014 · Cited by 505 · see citing works
Self-citationCharacterization of Peripheral Circadian Clocks in Adipose Tissues
Zvonic, S., Ptitsyn, A. A., Conrad, S. A., Scott, L. K., Floyd, Z. E., Kilroy, G. E., Wu, X., Goh, B. C. K., Mynatt, R. L., & Gimble, J. M. (2006) · Diabetes · doi:10.2337/diabetes.55.04.06.db05-0873 · Cited by 495 · see citing works
Clocks, metabolism, and the epigenome
Feng, D., & Lazar, M. A. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.06.026 · Cited by 271 · cited 3× · see citing works
“, regulation of hepatic gluconeogenesis and pancreatic b-cell insulin secretion (7).”
BackgroundMismatch of Sleep and Work Timing and Risk of Type 2 Diabetes
Vetter, C., Devore, E. E., Ramin, C. A., Speizer, F. E., Willett, W. C., & Schernhammer, E. S. (2015) · Diabetes Care · doi:10.2337/dc15-0302 · Cited by 195 · see citing works
Modeling Phasic Insulin Release
Nesher, R., & Cerasi, E. (2002) · Diabetes · doi:10.2337/diabetes.51.2007.s53 · Cited by 179 · see citing works
Jakubowicz, D. J., Wainstein, J., Åhrén, B., Landau, Z., Bar‐Dayan, Y., & Froy, O. (2015) · Diabetes Care · doi:10.2337/dc15-0761 · Cited by 172 · see citing works
Self-citationYasumoto, Y., Hashimoto, C., Nakao, R., Yamazaki, H., Hiroyama, H., Nemoto, T., Yamamoto, S., Sakurai, M., Oike, H., Wada, N., et al. (2016) · Metabolism · doi:10.1016/j.metabol.2016.02.003 · Cited by 168 · see citing works
AMPK at the crossroads of circadian clocks and metabolism
Jordan, S. D., & Lamia, K. A. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.06.017 · Cited by 162 · see citing works
Insulin secretory granules control autophagy in pancreatic β cells
Goginashvili, A., Zhang, Z., Erbs, E., Spiegelhalter, C., Kessler, P., Mihlan, M., Pasquier, A., Krupina, K., Schieber, N., Cinque, L., et al. (2015) · Science · doi:10.1126/science.aaa2628 · Cited by 160 · see citing works
Gunnarsson, P. T., Winzell, M. S., Deacon, C. F., Larsen, M. O., Jelic, K., Carr, R. D., & Åhrén, B. (2006) · Endocrinology · doi:10.1210/en.2005-1442 · Cited by 129 · see citing works
Clock gene expression in peripheral leucocytes of patients with type 2 diabetes
Ando, H., Takamura, T., Nagata, N., Shima, K. R., Eto, T., Misu, H., Shiramoto, M., Tsuru, T., Irie, S., Fujimura, A., et al. (2008) · Diabetologia · doi:10.1007/s00125-008-1194-6 · Cited by 124 · see citing works
Kudo, T., Akiyama, M., Kuriyama, K., Sudo, M., Moriya, T., & Shibata, S. (2004) · Diabetologia · doi:10.1007/s00125-004-1461-0 · Cited by 110 · see citing works
Sherman, H., Frumin, I., Gutman, R., Chapnik, N., Lorentz, A., Meylan, J., le Coutre, J., & Froy, O. (2010) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2010.01160.x · Cited by 109 · see citing works
Self-citationThe Second-Meal Phenomenon in Type 2 Diabetes
Jovanović, A., Gerrard, J., & Taylor, R. (2009) · Diabetes Care · doi:10.2337/dc08-2196 · Cited by 105 · see citing works
Wu, T., Sun, L., ZhuGe, F., Guo, X., Zhao, Z., Tang, R., Chen, Q., Chen, L., Kato, H., & Fu, Z. (2011) · Chronobiology International · doi:10.3109/07420528.2011.622599 · Cited by 86 · see citing works
Fuse, Y., Hirao, A., Kuroda, H., Otsuka, M., Tahara, Y., & Shibata, S. (2012) · Journal of Circadian Rhythms · doi:10.1186/1740-3391-10-4 · Cited by 79 · see citing works
Richards, J., Diaz, A. N., & Gumz, M. L. (2014) · Blood Pressure Monitoring · doi:10.1097/mbp.0000000000000060 · Cited by 72 · see citing works
Clock genes, pancreatic function, and diabetes
Vieira, E. C., Burris, T. P., & Quesada, I. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.10.007 · Cited by 68 · see citing works
Early nocturnal meal skipping alters the peripheral clock and increases lipogenesis in mice
Yoshida, C., Shikata, N., Seki, S., Koyama, N., & Noguchi, Y. (2012) · Nutrition & Metabolism · doi:10.1186/1743-7075-9-78 · Cited by 65 · see citing works
Pinho, A. V., Bensellam, M., Wauters, E., Rees, M., Giry-Laterrière, M., Mawson, A., Ly, L. Q., Biankin, A. V., Wu, J., Laybutt, D. R., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0128012 · Cited by 45 · see citing works
Wu, T., Ni, Y., Kato, H., & Fu, Z. (2010) · Chronobiology International · doi:10.3109/07420520903398625 · Cited by 45 · see citing works
Circadian clock gene expression is impaired in gestational diabetes mellitus
Pappa, K. I., Gazouli, M., Anastasiou, E., Iliodromiti, Z., Antsaklis, A. J., & Anagnou, N. P. (2013) · Gynecological Endocrinology · doi:10.3109/09513590.2012.743018 · Cited by 34 · see citing works
Ando, H., Ushijima, K., Yanagihara, H., Hayashi, Y., Takamura, T., Kaneko, S., & Fujimura, A. (2009) · Clinical and Experimental Hypertension · doi:10.1080/10641960902822450 · Cited by 29 · see citing works
Glucagon‐like peptide‐1: The missing link in the metabolic clock?
Brubaker, P. L., & Gil‐Lozano, M. (2016) · Journal of Diabetes Investigation · doi:10.1111/jdi.12477 · Cited by 29 · see citing works
Differential responses of peripheral circadian clocks to a short-term feeding stimulus
Wu, T., Fu, O., Yao, L., Sun, L., ZhuGe, F., & Fu, Z. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-1844-0 · Cited by 16 · see citing works
Kawakami, Y., Yamanaka‐Okumura, H., Sakuma, M., Mori, Y., Adachi, C., Matsumoto, Y., Sato, T., Yamamoto, H., Taketani, Y., Katayama, T., et al. (2013) · Lifestyle Genomics · doi:10.1159/000354247 · Cited by 15 · see citing works
Time-dependent Mechanisms in Beta-cell Glucose Sensing
Korsgaard, T. V., & Colding‐Jørgensen, M. (2006) · Journal of Biological Physics · doi:10.1007/s10867-006-9017-9 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The sirtuin family in health and disease
Wu, Q., Zhang, T., Chen, H., Yu, X., Lv, J.-L., Liu, Y., Liu, Y., Zheng, G., Zhao, J.-Q., Wei, Y., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01257-8 · Cited by 891 · see citing works
Jamshed, H., Beyl, R., Della Manna, D., Yang, E., Ravussin, E., & Peterson, C. (2019) · Nutrients · doi:10.3390/nu11061234 · Cited by 664 · see citing works
The circadian regulation of food intake
Challet, E. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0210-x · Cited by 428 · see citing works
Skipping breakfast is associated with overweight and obesity: A systematic review and meta-analysis
Ma, X., Chen, Q., Pu, Y., Guo, M., Jiang, Z., Huang, W., Long, Y., & Xu, Y. (2020) · Obesity Research & Clinical Practice · doi:10.1016/j.orcp.2019.12.002 · Cited by 293 · see citing works
Monzani, A., Ricotti, R., Caputo, M., Solito, A., Archero, F., Bellone, S., & Prodam, F. (2019) · Nutrients · doi:10.3390/nu11020387 · Cited by 274 · see citing works
Importance of circadian timing for aging and longevity
Acosta-Rodríguez, V. A., Rijo‐Ferreira, F., Green, C. B., & Takahashi, J. S. (2021) · Nature Communications · doi:10.1038/s41467-021-22922-6 · Cited by 249 · see citing works
Papakonstantinou, E., Oikonomou, C., Nychas, G., & Dimitriadis, G. D. (2022) · Nutrients · doi:10.3390/nu14040823 · Cited by 199 · see citing works
The Association between Chronotype and Dietary Pattern among Adults: A Scoping Review
Mazri, F. H., Manaf, Z. A., Shahar, S., & Mat Ludin, A. F. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17010068 · Cited by 198 · see citing works
van der Merwe, C., Münch, M. Y., & Kruger, R. (2022) · Advances in Nutrition · doi:10.1093/advances/nmac093 · Cited by 143 · see citing works
BaHammam, A. S., & Pirzada, R. (2023) · Clocks & Sleep · doi:10.3390/clockssleep5030034 · Cited by 138 · see citing works
Precision nutrition: A review of current approaches and future endeavors
Livingstone, K. M., Ramos-López, O., Përusse, L., Kato, H., Ordovás, J. M., & Martínez, J. A. (2022) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2022.08.017 · Cited by 136 · see citing works
Lundell, L. S., Parr, E. B., Devlin, B. L., Ingerslev, L. R., Altıntaş, A., Sato, S., Sassone‐Corsi, P., Barrès, R., Zierath, J. R., & Hawley, J. A. (2020) · Nature Communications · doi:10.1038/s41467-020-18412-w · Cited by 133 · see citing works
The Microbiota and the Gut–Brain Axis in Controlling Food Intake and Energy Homeostasis
Romaní‐Pérez, M., Bullich‐Vilarrubias, C., López‐Almela, I., Liébana-García, R., Olivares, M., & Sanz, Y. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115830 · Cited by 113 · see citing works
Circadian Synchrony: Sleep, Nutrition, and Physical Activity
Healy, K. L., Morris, A. R., & Liu, A. C. (2021) · Frontiers in Network Physiology · doi:10.3389/fnetp.2021.732243 · Cited by 90 · see citing works
The Big Breakfast Study: Chrono‐nutrition influence on energy expenditure and bodyweight
Ruddick-Collins, L. C., Johnston, J. D., Morgan, P. J., & Johnstone, A. M. (2018) · Nutrition Bulletin · doi:10.1111/nbu.12323 · Cited by 87 · see citing works
Coupling the Circadian Clock to Homeostasis: The Role of Period in Timing Physiology
Kim, P., Oster, H., Lehnert, H., Schmid, S. M., Salamat, N., Barclay, J. L., Maronde, E., Inder, W. J., & Rawashdeh, O. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00049 · Cited by 83 · see citing works
Alam, I., Gul, R., Chong, J., Tan, C. T. Y., Chin, H. X., Wong, G. C. L., Doggui, R., & Larbi, A. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-019-2007-z · Cited by 82 · see citing works
Jakubowicz, D. J., Landau, Z., Tsameret, S., Wainstein, J., Raz, I., Åhrén, B., Chapnik, N., Barnea, M., Ganz, T., Menaged, M., et al. (2019) · Diabetes Care · doi:10.2337/dc19-1142 · Cited by 78 · see citing works
Self-citationHaupt, S., Eckstein, M. L., Wolf, A., Zimmer, R. T., Wachsmuth, N. B., & Moser, O. (2021) · Biomolecules · doi:10.3390/biom11040516 · Cited by 69 · see citing works
Raji, O. E., Kyeremah, E., Sears, D. D., St‐Onge, M., & Makarem, N. (2024) · Nutrients · doi:10.3390/nu16142332 · Cited by 60 · see citing works
The effect of breakfast on childhood obesity: a systematic review and meta-analysis
Wang, K., Niu, Y., Lu, Z., Duo, B., Effah, C. Y., & Guan, L. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1222536 · Cited by 56 · see citing works
Maugeri, A., Kunzová, Š., Medina‐Inojosa, J. R., Agodi, A., Barchitta, M., Homolka, M., Kiacova, N., Bauerová, H., Sochor, O., López-Jiménez, F. A., et al. (2018) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2018.04.002 · Cited by 55 · see citing works
Jakubowicz, D. J., Wainstein, J., Tsameret, S., & Landau, Z. (2021) · Nutrients · doi:10.3390/nu13051558 · Cited by 54 · see citing works
Self-citationNutrient timing and metabolic regulation
Smith, H. A., & Betts, J. A. (2022) · The Journal of Physiology · doi:10.1113/jp280756 · Cited by 54 · see citing works
Circadian Regulation of Metabolism: Commitment to Health and Diseases
Sato, T., & Sato, S. (2023) · Endocrinology · doi:10.1210/endocr/bqad086 · Cited by 50 · see citing works
Allison, K. C., & Goel, N. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.02.047 · Cited by 49 · see citing works
Efficacy of Dietary and Supplementation Interventions for Individuals with Type 2 Diabetes
Lewgood, J., Oliveira, B., Korzepa, M., Forbes, S. C., Little, J. P., Breen, L., Bailie, R., & Candow, D. G. (2021) · Nutrients · doi:10.3390/nu13072378 · Cited by 49 · see citing works
Dose, B., Yalçın, M., Dries, S. P. M., & Relógio, A. (2023) · Frontiers in Digital Health · doi:10.3389/fdgth.2023.1157654 · Cited by 46 · see citing works
Chrononutrition in type 2 diabetes mellitus and obesity: A narrative review
Verde, L., Lorenzo, T. D., Savastano, S., Colao, A., Barrea, L., & Muscogiuri, G. (2024) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3778 · Cited by 46 · see citing works
de Souza, M. R., Neves, M. E. A., Souza, A. D. M., Muraro, A. P., Pereira, R. A., Ferreira, M. G., & Rodrigues, P. R. M. (2020) · British Journal Of Nutrition · doi:10.1017/s0007114520003992 · Cited by 46 · see citing works
Chen, J.-H., Lu, L. W., Ge, Q., Feng, D., Yu, J., Liu, B., Zhang, R., Zhang, X., Ouyang, C., & Chen, F. (2023) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1974335 · Cited by 45 · see citing works
Cros, A. P., Srour, B., Andreeva, V. A., Fezeu, L., Bellicha, A., Kesse‐Guyot, E., Herçberg, S., Romaguera, D., Kogevinas, M., & Touvier, M. (2023) · International Journal of Epidemiology · doi:10.1093/ije/dyad081 · Cited by 45 · see citing works
The importance of being rhythmic: Living in harmony with your body clocks
Dibner, C. (2019) · Acta Physiologica · doi:10.1111/apha.13281 · Cited by 45 · see citing works
Liu, B., Hutchison, A. T., Thompson, C. H., Lange, K., Wittert, G. A., & Heilbronn, L. K. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa707 · Cited by 39 · see citing works
Gwin, J. A., & Leidy, H. J. (2018) · Advances in Nutrition · doi:10.1093/advances/nmy047 · Cited by 37 · see citing works
Santos, H. O., Genário, R., Macedo, R. C. O., Pareek, M., & Tinsley, G. M. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1819768 · Cited by 37 · see citing works
Ogata, H., Horie, M., Kayaba, M., Tanaka, Y., Ando, A., Park, I., Zhang, S., Yajima, K., Shoda, J., Omi, N., et al. (2020) · Nutrients · doi:10.3390/nu12092797 · Cited by 34 · see citing works
Tsameret, S., Chapnik, N., & Froy, O. (2023) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-023-04834-4 · Cited by 31 · see citing works
Self-citationRizza, S., Luzi, A., Mavilio, M., Ballanti, M., Massimi, A., Porzio, O., Magrini, A., Hannemann, J., Menghini, R., Lehrke, M., et al. (2021) · Acta Diabetologica · doi:10.1007/s00592-021-01676-z · Cited by 31 · see citing works
Mustafa, N., Majid, H. A., Toumpakari, Z., Carroll, H. A., Jalaludin, M. Y., Al-Sadat, N., & Johnson, L. (2019) · Nutrients · doi:10.3390/nu11050973 · Cited by 31 · see citing works
Reprint of: Precision nutrition: A review of current approaches and future endeavors
Livingstone, K. M., Ramos-López, O., Përusse, L., Kato, H., Ordovás, J. M., & Martínez, J. A. (2022) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2022.10.010 · Cited by 30 · see citing works
Chronobiology and Metabolism: Is Ketogenic Diet Able to Influence Circadian Rhythm?
Gangitano, E., Gnessi, L., Lenzi, A., & Ray, D. W. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.756970 · Cited by 30 · see citing works
Influence of obesity, weight loss, and free fatty acids on skeletal muscle clock gene expression
Puig, L. S., Pillon, N. J., Näslund, E. B., Krook, A., & Zierath, J. R. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00289.2019 · Cited by 30 · see citing works
Alsalim, W., Lindgren, O., & Åhrén, B. (2022) · Journal of Diabetes Investigation · doi:10.1111/jdi.13962 · Cited by 29 · see citing works
Intermittent fasting: What questions should we be asking?
Liu, K., Liu, B., & Heilbronn, L. K. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112827 · Cited by 29 · see citing works
Messika, A., Toledano, Y., Hadar, E., Shmuel, E., Tauman, R., Shamir, R., & Froy, O. (2022) · American Journal of Obstetrics & Gynecology MFM · doi:10.1016/j.ajogmf.2022.100660 · Cited by 28 · see citing works
Self-citationFiore, G., Scapaticci, S., Neri, C. R., Azaryah, H., Escudero-Marín, M., Pascuzzi, M. C., Mendola, A. L., Mameli, C., Chiarelli, F., Campoy, C., et al. (2023) · Nutrition Reviews · doi:10.1093/nutrit/nuad122 · Cited by 27 · see citing works
Dong, J.-Y., Ikehara, S., Kimura, T., Cui, M., Kawanishi, Y., Kimura, T., Ueda, K., & Iso, H. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa014 · Cited by 26 · see citing works
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Díaz, X., & Quintiliano, D. A. (2020) · Nutrients · doi:10.3390/nu12020552 · Cited by 24 · see citing works
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Cecchini, A. L., Biscetti, F., Rando, M. M., Nardella, E., Pecorini, G., Eraso, L. H., DiMuzio, P. J., Gasbarrini, A., Massetti, M., & Flex, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810814 · Cited by 24 · see citing works
Peng, J., Lu, J., Ma, X., Ying, L., Lu, W., Zhu, W., Bao, Y., & Zhou, J. (2018) · British Journal Of Nutrition · doi:10.1017/s0007114518003628 · Cited by 24 · see citing works
Minimally Invasive Ways of Determining Circadian Rhythms in Humans
Crnko, S., Schutte, H., Doevendans, P. A., Sluijter, J. P. G., & Laake, L. W. V. (2020) · Physiology · doi:10.1152/physiol.00018.2020 · Cited by 24 · see citing works
Akbar, Z., & Shi, Z. (2024) · Nutrients · doi:10.3390/nu16111581 · Cited by 23 · see citing works
Helo, D., Appiah, L., Bhende, K., Byrd, T. L., & Appiah, D. (2021) · Cancer Causes & Control · doi:10.1007/s10552-021-01401-9 · Cited by 23 · see citing works
Disruption of the circadian rhythms and its relationship with pediatric obesity
Kawai, M. (2021) · Pediatrics International · doi:10.1111/ped.14992 · Cited by 22 · see citing works
ALTAMIMI, J. Z., Alshwaiyat, N. M., Alkhalidy, H., AlFaris, N. A., AlKehayez, N. M., & Alagal, R. I. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19052903 · Cited by 22 · see citing works
Attention to Innate Circadian Rhythm and the Impact of Its Disruption on Diabetes
Lee, D. Y., Jung, I., Park, S. Y., Yu, J. H., Seo, J. A., Kim, K. J., Kim, N. H., Yoo, H. J., Kim, S. G., Choi, K. M., et al. (2024) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2023.0193 · Cited by 21 · see citing works
Xie, J., Huang, H., Chen, Y., Xu, L., & Xu, C. (2021) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.16727 · Cited by 21 · see citing works
Morning Hyperinsulinemia Primes the Liver for Glucose Uptake and Glycogen Storage Later in the Day
Moore, M. C., Smith, M. S., Farmer, B., Coate, K. C., Kraft, G., Shiota, M., Williams, P. E., & Cherrington, A. D. (2018) · Diabetes · doi:10.2337/db17-0979 · Cited by 21 · see citing works
Circadian misalignment in obesity: The role for time-restricted feeding
Chambers, L., Seidler, K., & Barrow, M. (2023) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2023.07.086 · Cited by 20 · see citing works
Maugeri, A., & Vinciguerra, M. (2020) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2020.9.1.140 · Cited by 20 · see citing works
Heo, J., Choi, W., Ham, S., Kang, S., & Lee, W. (2021) · Nutrition & Metabolism · doi:10.1186/s12986-020-00526-z · Cited by 20 · see citing works
Zhou, L., Kang, L., Xiao, X., Jia, L., Zhang, Q., & Deng, M. (2019) · International Journal of Endocrinology · doi:10.1155/2019/5893028 · Cited by 19 · see citing works
Influence of lifestyle and the circadian clock on reproduction
Ono, M., Dai, Y., Fujiwara, T., Fujiwara, H., Daikoku, T., Ando, H., Kuji, N., & Nishi, H. (2025) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12641 · Cited by 18 · see citing works
Zhao, L., Teong, X. T., Liu, K., Liu, B., Melaku, Y. A., Vincent, A. D., Manoogian, E. N. C., Panda, S., Wittert, G., Hutchison, A. T., et al. (2021) · British Journal Of Nutrition · doi:10.1017/s0007114521002944 · Cited by 18 · see citing works
Barua, S., Sabharwal, A., GLANTZ, N. M., Conneely, C., LAREZ, A. J., Bevier, W. C., & Kerr, D. E. (2021) · EClinicalMedicine · doi:10.1016/j.eclinm.2021.101241 · Cited by 18 · see citing works
Nutritional entrainment of circadian rhythms under alignment and misalignment: A mechanistic review
Chambers, L., Seidler, K., & Barrow, M. (2022) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2022.06.010 · Cited by 18 · see citing works
Hatamoto, Y., Tanoue, Y., Yoshimura, E., Matsumoto, M., Hayashi, T., Ogata, H., Tanaka, S., Tanaka, H., & Higaki, Y. (2023) · Journal of Nutrition · doi:10.1016/j.tjnut.2022.12.024 · Cited by 17 · see citing works
Wang, Y., Li, F., Li, X., Wu, J., Chen, X., Su, Y., Qin, T., Liu, X., Liang, L., Jianping, M., et al. (2024) · Food & Function · doi:10.1039/d3fo05705d · Cited by 17 · see citing works
Jakubowicz, D. J., Rosenblum, R. C., Wainstein, J., & Twito, O. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087154 · Cited by 16 · see citing works
Self-citationJabri, L., Alrasheedi, A. A., Alsulaimani, R. A., & Al-Hazzaa, H. M. (2021) · Children · doi:10.3390/children8020134 · Cited by 16 · see citing works
Timing of energy intake and BMI in children: differential impacts by age and sex
Mahdi, S., Dickerson, A. P., Solar, G. I., & Caton, S. J. (2022) · British Journal Of Nutrition · doi:10.1017/s0007114522003014 · Cited by 15 · see citing works
The circadian rhythm as therapeutic target in inflammatory bowel disease
Post, Z., Zilberstein, N., & Keshavarzian, A. (2024) · Journal of the Canadian Association of Gastroenterology · doi:10.1093/jcag/gwae027 · Cited by 15 · see citing works
AlFaris, N. A., Alshwaiyat, N. M., Alkhalidy, H., Alagal, R. I., ALTAMIMI, J. Z., & AlKehayez, N. M. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2021.761383 · Cited by 15 · see citing works
Chrono‐nutrition for hypertension
Bohmke, N. J., Dixon, D. L., & Kirkman, D. L. (2024) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3760 · Cited by 15 · see citing works
Lages, M., Carmo‐Silva, S., Barros, R., & Guarino, M. P. (2024) · Proceedings of The Nutrition Society · doi:10.1017/s002966512400747x · Cited by 14 · see citing works
Sun, M., Wang, X., Wang, L., Hu, W., Yang, Y., Yao, N., Li, J., Xie, Z., Guo, R., Wang, Y., et al. (2022) · Nutrients · doi:10.3390/nu14204378 · Cited by 13 · see citing works
The role of circadian gene CLOCK in cancer
Rashed, N., Liu, W., Zhou, X., Bode, A. M., & Luo, X. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2024.119782 · Cited by 12 · see citing works
Jakubowicz, D. J., Matz, Y., Landau, Z., Rosenblum, R. C., Twito, O., Wainstein, J., & Tsameret, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252212355 · Cited by 12 · see citing works
Self-citationAslam, M., Madhu, S. V., Keithellakpam, K., Mehndiratta, M., Mishra, B., & Neh, V. (2021) · Chronobiology International · doi:10.1080/07420528.2021.1881108 · Cited by 12 · see citing works
Miyamura, K., Nawa, N., Isumi, A., Doi, S. K., Ochi, M., & Fujiwara, T. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1051592 · Cited by 11 · see citing works
Intemann, T., Bogl, L. H., Hunsberger, M. L., Lauria, F., Henauw, S. D., Molnár, D., Moreno, L. A., Tornaritis, M. J., Veidebaum, T., Ahrens, W., et al. (2024) · Pediatric Diabetes · doi:10.1155/2024/6623357 · Cited by 11 · see citing works
Breakfast Frequency Is Inversely Associated with Weight Gain in a Cohort of Mexican Women
Martínez, C. F., Ortiz‐Panozo, E., Mattei, J., Campos, H., Flores, M., & Lajous, M. (2020) · Journal of Nutrition · doi:10.1093/jn/nxaa367 · Cited by 11 · see citing works
Cros, A. P., Harding, B. N., Espinosa, A., Papantoniou, K., Pérez‐Gómez, B., Straíf, K., Ardanáz, E., Fernández‐Villa, T., Amiano, P., Gómez‐Acebo, I., et al. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.941477 · Cited by 11 · see citing works
Clayton, D. J., Mode, W. J. A., & Slater, T. (2020) · Nutrition Bulletin · doi:10.1111/nbu.12467 · Cited by 11 · see citing works
New insights into the mechanisms of diabetic kidney disease: Role of circadian rhythm and Bmal1
Peng, Z., Liang, Y., Liu, X., Shao, J., Hu, N., & Zhang, X. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115422 · Cited by 9 · see citing works
Bonham, M. P., Kaias, E., Huggins, C. E., Davis, R., Leung, G. K. W., Eikelis, N., Shaw, E., & Murgia, C. (2019) · Clinical Nutrition · doi:10.1016/j.clnu.2019.02.018 · Cited by 9 · see citing works
Zhao, L., Hutchison, A. T., Wittert, G., Thompson, C. H., Lange, K. M., Liu, B., & Heilbronn, L. K. (2020) · Obesity · doi:10.1002/oby.22775 · Cited by 9 · see citing works
Tanaka, K., Kawakami, S., Mori, S., Yamaguchi, T., Saito, E., Setoguchi, Y., Matsui, Y., Nishimura, E., Ebihara, S., & Kawama, T. (2024) · Life · doi:10.3390/life14050589 · Cited by 8 · see citing works
Smith, H., Watkins, J. D., Walhin, J., Gonzalez, J. T., Thompson, D., & Betts, J. A. (2023) · Journal of Nutrition · doi:10.1016/j.tjnut.2023.08.008 · Cited by 8 · see citing works
ElDash, R. M., Raslan, M. A., Shaheen, S. M., & Sabri, N. A. (2021) · F1000Research · doi:10.12688/f1000research.51114.1 · Cited by 8 · see citing works
Aizawa, M., Murakami, K., Takahashi, I., Onuma, T., Noda, A., Ueno, F., Matsuzaki, F., Ishikuro, M., Obara, T., Hamada, H., et al. (2023) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-023-05603-8 · Cited by 8 · see citing works
Jiang, W., Song, Q., Zhang, J., Chen, Y., Jiang, H., Long, Y., Li, Y., Han, T., Sun, H., & Wei, W. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac069 · Cited by 8 · see citing works
Eom, H., Lee, D., Cho, Y., & Moon, J. (2022) · Nutrition Research and Practice · doi:10.4162/nrp.2022.16.2.205 · Cited by 7 · see citing works
Malik, M. Z., DASHTI, M. H., Fatima, Y., Channanath, A. M., John, S. E., Singh, R. K. B., Al‐Mulla, F., & Thanaraj, T. A. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1217992 · Cited by 7 · see citing works
Breakfast skipping and traits of cardiometabolic health: A mendelian randomization study
Meng, X., Zhong, Y., Peng, Y., & Qian, C. (2023) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2023.12.149 · Cited by 7 · see citing works
Messika, A., Toledano, Y., Hadar, E., Tauman, R., Froy, O., & Shamir, R. (2024) · Nutrients · doi:10.3390/nu17010157 · Cited by 7 · see citing works
Self-citationBravo-García, A. P., Radford, B. E., Hall, R. C., Broome, S. C., Tee, N., Arthur, B., Janssens, K., Johnston, R. D., Halson, S. L., Devlin, B. L., et al. (2025) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2025.112081 · Cited by 7 · see citing works
Fischer, J. A. J., Thomas, J. G., Ierodiakonou, D., van Zutphen, K. G., & García-Larsen, V. (2025) · Campbell Systematic Reviews · doi:10.1002/cl2.70039 · Cited by 7 · see citing works
Delgado-Alarcón, J. M., Morante, J. J. H., Avilés, F., Albaladejo-Otón, M. D., & Morillas-Ruiz, J. M. (2020) · Nutrients · doi:10.3390/nu12061695 · Cited by 7 · see citing works
- Authors
- Jakubowicz, D., Wainstein, J., Landau, Z., Raz, I., Ahren, B., Chapnik, N., Ganz, T., Menaged, M., Barnea, M., Bar-Dayan, Y., & Froy, O.
- Affiliations
- Tel Aviv University (IL)
- Hebrew University of Jerusalem (IL)
- Department of Clinical Sciences, Faculty of Medicine, Lund University, Lund, Sweden
- Weizmann Institute of Science (IL)
- Diabetes Unit, Wolfson Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Holon, Israel
- Corresponding author
- Jakubowicz, Daniela
- Froy, Oren
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2017-08-22
- Volume
- 40
- Issue
- 11
- Pages
- 1573-1579
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- OpenAlex
- W2745443951
- Cited by
- 178
- References
- 39
- Citations by year
- 2026: 10 · 2025: 19 · 2024: 28 · 2023: 24 · 2022: 25 · 2021: 26 · 2020: 21 · 2019: 16 · 2018: 8 · 2017: 1
- FWCI
- 7.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes Care (publishedVersion)
- PubMed (publishedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Funders
- Ministry of Health, Israel (3-0000-11406)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Physiology › Dietary Effects on Health
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Keywords
- breakfast skipping, clock genes, circadian clock, postprandial blood glucose, type 2 diabetes, glucose homeostasis, Per1, Per2, Bmal1, RORα, SIRT1, glucagon-like peptide-1, dipeptidyl peptidase IV, insulin, circadian rhythm
- MeSH terms
- Adult, Aged, Blood Glucose, Diabetes Mellitus, Type 2, Gene Expression Regulation, Glycated Hemoglobin, Homeostasis, Humans, Insulin, Middle Aged, Body Mass Index, Cross-Over Studies, Postprandial Period, Glucagon-Like Peptide 1, AMP-Activated Protein Kinases, Sirtuin 1, ARNTL Transcription Factors, Period Circadian Proteins, Circadian Clocks, Breakfast
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