Circadian rhythms, metabolism, and chrononutrition in rodents and humans

Advances in Nutrition

Volumn 7, Issue 2, 2016, Pages 399-406

  Johnston, Jonathan D ^a   Ordovás, José M ^b,c   Scheer, Frank A ^d,e   Turek, Fred W ^f  

^a UNIVERSITY OF SURREY   (United Kingdom)

^b TUFTS UNIVERSITY   (United States)

^c IMDEA FOOD INSTITUTE   (Spain)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Chronobiology; Clock gene; Diabetes; Dietary patterns; Eating behavior; Genetics; Meal timing; Metabolic syndrome; Misalignment; Obesity

Indexed keywords

NERVE PROTEIN; TRANSCRIPTION FACTOR CLOCK;

ANIMAL; ANIMAL FOOD; CHRONOBIOLOGY; CIRCADIAN RHYTHM; COMPARATIVE STUDY; ENERGY METABOLISM; GENETIC VARIATION; GENETICS; HUMAN; MEAL; METABOLIC SYNDROME X; METABOLISM; MOUSE; MUTANT MOUSE STRAIN; NERVE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NUTRITION; ORGANIZATION; RAT; SUPRACHIASMATIC NUCLEUS; TRANSGENIC MOUSE;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CHRONOBIOLOGY PHENOMENA; CIRCADIAN RHYTHM; CLOCK PROTEINS; CONGRESSES AS TOPIC; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; GENETIC VARIATION; HUMANS; MEALS; METABOLIC SYNDROME X; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; RATS; SUPRACHIASMATIC NUCLEUS;

EID: 84961668078     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.115.010777     Document Type: Article

References (96)

1. Pittendrigh CS. Temporal organization: reflections of a Darwinian clock-watcher. Annu Rev Physiol 1993;55:16-54.
2. Skene DJ, Arendt J. Human circadian rhythms: physiological and therapeutic relevance of light and melatonin. Ann Clin Biochem 2006;43:344-53.
3. Inouye ST, Kawamura H. Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA 1979;76:5962-6.
4. Green DJ, Gillette R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 1982;245:198-200.
5. Stephan FK, Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 1972;69:1583-6.
6. Moore RY, Eichler VB. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 1972;42:201-6.
7. Ralph MR, Foster RG, Davis FC, Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science 1990;247:975-8.
8. Lamia KA, Storch KF, Weitz CJ. Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci USA 2008;105:15172-7.
9. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH, et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 2010;466:627-31.
10. Sadacca LA, Lamia KA, deLemos AS, Blum B, Weitz CJ. An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia 2011;54:120-4.
11. Peschke E, Peschke D. Evidence for a circadian rhythm of insulin release from perifused rat pancreatic islets. Diabetologia 1998;41:1085-92.
12. Paschos GK, Ibrahim S, Song WL, Kunieda T, Grant G, Reyes TM, Bradfield CA, Vaughan CH, Eiden M, Masoodi M, et al. Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med 2012;18:1768-77.
13. Shostak A, Meyer-Kovac J, Oster H. Circadian regulation of lipid mobilization in white adipose tissues. Diabetes 2013;62:2195-203.
14. Dyar KA, Ciciliot S, Wright LE, Bienso RS, Tagliazucchi GM, Patel VR, Forcato M, Paz MI, Gudiksen A, Solagna F, et al. Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock. Mol Metab 2014;3:29-41.
15. Lucas RJ, Lall GS, Allen AE, Brown TM. How rod, cone, and melanopsin photoreceptors come together to enlighten the mammalian circadian clock. Prog Brain Res 2012;199:1-18.
16. Albrecht U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 2012;74:246-60.
17. Laing EE, Johnston JD, Moller-Levet CS, Bucca G, Smith CP, Dijk DJ, Archer SN. Exploiting human and mouse transcriptomic data: Identification of circadian genes and pathways influencing health. BioEssays 2015;37:544-56.
18. Husse J, Leliavski A, Tsang AH, Oster H, Eichele G. The light-dark cycle controls peripheral rhythmicity in mice with a genetically ablated suprachiasmatic nucleus clock. FASEB J 2014;28:4950-60.
19. Partch CL, Green CB, Takahashi JS. Molecular architecture of the mammalian circadian clock. Trends Cell Biol 2014;24:90-9.
20. Lim C, Allada R. Emerging roles for post-transcriptional regulation in circadian clocks. Nat Neurosci 2013;16:1544-50.
21. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002;110:251-60.
22. Canaple L, Rambaud J, Dkhissi-Benyahya O, Rayet B, Tan NS, Michalik L, Delaunay F, Wahli W, Laudet V. Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferator-activated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock. Mol Endocrinol 2006;20:1715-27.
23. Sassone-Corsi P. Minireview: NAD+, a circadian metabolite with an epigenetic twist. Endocrinology 2012;153:1-5.
24. Peek CB, Ramsey KM, Levine DC, Marcheva B, Perelis M, Bass J. Circadian regulation of cellular physiology. Methods Enzymol 2015;552:165-84.
25. O'Neill JS, Maywood ES, Hastings MH. Cellular mechanisms of circadian pacemaking: beyond transcriptional loops. Handb Exp Pharmacol 2013(217):67-103.
26. Milev NB, Reddy AB. Circadian redox oscillations and metabolism. Trends Endocrinol Metab 2015;26:430-7.
27. Jin X, Shearman LP, Weaver DR, Zylka MJ, de Vries GJ, Reppert SM. A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell 1999;96:57-68.
28. Ripperger JA, Shearman LP, Reppert SM, Schibler U. CLOCK, an essential pacemaker component, controls expression of the circadian transcription factor DBP. Genes Dev 2000;14:679-89.
29. Duffield GE. DNA microarray analyses of circadian timing: the genomic basis of biological time. J Neuroendocrinol 2003;15:991-1002.
30. Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB. A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci USA 2014;111:16219-24.
31. Möller-Levet CS, Archer SN, Bucca G, Laing EE, Slak A, Kabiljo R, Lo JC, Santhi N, von Schantz M, Smith CP, et al. Effects of insufficient sleep on circadian rhythmicity and expression amplitude of the human blood transcriptome. Proc Natl Acad Sci USA 2013;110:E1132-41.
32. Archer SN, Laing EE, Moller-Levet CS, van der Veen DR, Bucca G, Lazar AS, Santhi N, Slak A, Kabiljo R, von Schantz M, et al. Mistimed sleep disrupts circadian regulation of the human transcriptome. Proc Natl Acad Sci USA 2014;111:E682-91.
33. Deery MJ, Maywood ES, Chesham JE, Sladek M, Karp NA, Green EW, Charles PD, Reddy AB, Kyriacou CP, Lilley KS, et al. Proteomic analysis reveals the role of synaptic vesicle cycling in sustaining the suprachiasmatic circadian clock. Curr Biol 2009;19:2031-6.
34. Chiang CK, Mehta N, Patel A, Zhang P, Ning Z, Mayne J, Sun WY, Cheng HY, Figeys D. The proteomic landscape of the suprachiasmatic nucleus clock reveals large-scale coordination of key biological processes. PLoS Genet 2014;10:e1004695.
35. Reddy AB, Karp NA, Maywood ES, Sage EA, Deery M, O'Neill JS,Wong GK, Chesham J, Odell M, Lilley KS, et al. Circadian orchestration of the hepatic proteome. Curr Biol 2006;16:1107-15.
36. Mauvoisin D, Wang J, Jouffe C, Martin E, Atger F, Waridel P, Quadroni M, Gachon F, Naef F. Circadian clock-dependent and -independent rhythmic proteomes implement distinct diurnal functions in mouse liver. Proc Natl Acad Sci USA 2014;111:167-72.
37. Robles MS, Cox J, Mann M. In-vivo quantitative proteomics reveals a key contribution of post-transcriptional mechanisms to the circadian regulation of liver metabolism. PLoS Genet 2014;10:e1004047.
38. Lück S, Thurley K, Thaben PF, Westermark PO. Rhythmic degradation explains and unifies circadian transcriptome and proteome data. Cell Reports 2014;9:741-51.
39. Minami Y, Kasukawa T, Kakazu Y, Iigo M, Sugimoto M, Ikeda S, Yasui A, van der Horst GT, Soga T, Ueda HR. Measurement of internal body time by blood metabolomics. Proc Natl Acad Sci USA 2009;106:9890-5.
40. Eckel-Mahan KL, Patel VR, Mohney RP, Vignola KS, Baldi P, Sassone-Corsi P. Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci USA 2012;109:5541-6.
41. Fustin JM, Doi M, Yamada H, Komatsu R, Shimba S, Okamura H. Rhythmic nucleotide synthesis in the liver: temporal segregation of metabolites. Cell Reports 2012;1:341-9.
42. Hatori M, Vollmers C, Zarrinpar A, DiTacchio L, Bushong EA, Gill S, Leblanc M, Chaix A, Joens M, Fitzpatrick JA, et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 2012;15:848-60.
43. Castro C, Briggs W, Paschos GK, FitzGerald GA, Griffin JL. A metabolomic study of adipose tissue in mice with a disruption of the circadian system. Mol Biosyst 2015;11:1897-906.
44. Dallmann R, Viola AU, Tarokh L, Cajochen C, Brown SA. The human circadian metabolome. Proc Natl Acad Sci USA 2012;109:2625-9.
45. Ang JE, Revell V, Mann A, Mantele S, Otway DT, Johnston JD, Thumser AE, Skene DJ, Raynaud F. Identification of human plasma metabolites exhibiting time-of-day variation using an untargeted liquid chromatography-mass spectrometry metabolomic approach. Chronobiol Int 2012;29:868-81.
46. Davies SK, Ang JE, Revell VL, Holmes B, Mann A, Robertson FP, Cui N, Middleton B, Ackermann K, Kayser M, et al. Effect of sleep deprivation on the human metabolome. Proc Natl Acad Sci USA 2014;111:10761-6.
47. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS. Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 1994;264:719-25.
48. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 2005;308:1043-5.
49. Summa KC, Turek FW. Chronobiology and obesity: Interactions between circadian rhythms and energy regulation. Adv Nutr 2014;5:312S-9S.
50. Linkowski P, Van Onderbergen A, Kerkhofs M, Bosson D, Mendlewicz J, Van Cauter E. Twin study of the 24-h cortisol profile: evidence for genetic control of the human circadian clock. Am J Physiol 1993;264: E173-81.
51. Scott EM, Carter AM, Grant PJ. Association between polymorphisms in the Clock gene, obesity and the metabolic syndrome in man. Int J Obes (Lond) 2008;32:658-62.
52. Monteleone P, Tortorella A, Docimo L, Maldonato MN, Canestrelli B, De Luca L, Maj M. Investigation of 3111T/C polymorphism of the CLOCK gene in obese individuals with or without binge eating disorder: association with higher body mass index. Neurosci Lett 2008;435:30-3.
53. Garaulet M, Lee YC, Shen J, Parnell LD, Arnett DK, Tsai MY, Lai CQ, Ordovas JM. CLOCK genetic variation and metabolic syndrome risk: modulation by monounsaturated fatty acids. Am J Clin Nutr 2009;90:1466-75.
54. Dashti HS, Aslibekyan S, Scheer FA, Smith CE, Lamon-Fava S, Jacques P, Lai CQ, Tucker KL, Arnett DK, Ordovas JM. Clock genes explain a large proportion of phenotypic variance in systolic blood pressure and this control is not modified by environmental temperature. Am J Hypertens 2015;29:132-40.
55. Garaulet M, Lee YC, Shen J, Parnell LD, Arnett DK, Tsai MY, Lai CQ, Ordovas JM. Genetic variants in human CLOCK associate with total energy intake and cytokine sleep factors in overweight subjects (GOLDN population). Eur J Hum Genet 2010;18:364-9.
56. Garaulet M, Corbalan MD, Madrid JA, Morales E, Baraza JC, Lee YC, Ordovas JM. CLOCK gene is implicated in weight reduction in obese patients participating in a dietary programme based on the Mediterranean diet. Int J Obes (Lond) 2010;34:516-23.
57. Garaulet M, Sanchez-Moreno C, Smith CE, Lee YC, Nicolas F, Ordovas JM. Ghrelin, sleep reduction and evening preference: relationships to CLOCK 3111 T/C SNP and weight loss. PLoS One 2011;6:e17435.
58. Dashti HS, Smith CE, Lee YC, Parnell LD, Lai CQ, Arnett DK, Ordovas JM, Garaulet M. CRY1 circadian gene variant interacts with carbohydrate intake for insulin resistance in two independent populations: Mediterranean and North American. Chronobiol Int 2014;31:660-7.
59. Garcia-Rios A, Perez-Martinez P, Delgado-Lista J, Phillips CM, Gjelstad IM, Wright JW, KarlstromB, Kiec-Wilk B, vanHeesAM, HelalO, et al. A Period 2 genetic variant interacts with plasma SFA to modify plasma lipid concentrations in adults with metabolic syndrome. J Nutr 2012;142:1213-8.
60. Garaulet M, Corbalan-Tutau MD, Madrid JA, Baraza JC, Parnell LD, Lee YC, Ordovas JM. PERIOD2 variants are associated with abdominal obesity, psycho-behavioral factors, and attrition in the dietary treatment of obesity. J Am Diet Assoc 2010;110:917-21.
61. Garaulet M, Esteban Tardido A, Lee YC, Smith CE, Parnell LD, Ordovas JM. SIRT1 and CLOCK 3111T> C combined genotype is associated with evening preference and weight loss resistance in a behavioral therapy treatment for obesity. Int J Obes (Lond) 2012;36:1436-41.
62. Karthikeyan R, Marimuthu G, Sooriyakumar M. BaHammam AS, Spence DW, Pandi-Perumal SR, Brown GM, Cardinali DP. Per3 length polymorphism in patients with type 2 diabetes mellitus. Horm Mol Biol Clin Investig 2014;18:145-9.
63. Morris CJ, Yang JN, Scheer FA. The impact of the circadian timing system on cardiovascular and metabolic function. Prog Brain Res 2012;199:337-58.
64. Antunes LC, Levandovski R, Dantas G, CaumoW, Hidalgo MP. Obesity and shift work: chronobiological aspects. Nutr Res Rev 2010;23:155-68.
65. Lowden A, Moreno C, Holmback U, Lennernas M, Tucker P. Eating and shift work - effects on habits, metabolism and performance. Scand J Work Environ Health 2010;36:150-62.
66. Tucker P, Marquie JC, Folkard S, Ansiau D, Esquirol Y. Shiftwork and metabolic dysfunction. Chronobiol Int 2012;29:549-55.
67. Hampton SM, Morgan LM, Lawrence N, Anastasiadou T, Norris F, Deacon S, Ribeiro D, Arendt J. Postprandial hormone and metabolic responses in simulated shift work. J Endocrinol 1996;151:259-67.
68. Lund J, Arendt J, Hampton SM, English J, Morgan LM. Postprandial hormone and metabolic responses amongst shift workers in Antarctica. J Endocrinol 2001;171:557-64.
69. Scheer FA, Hilton MF, Mantzoros CS, Shea SA. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci USA 2009;106:4453-8.
70. Buxton OM, Cain SW, O'Connor SP, Porter JH, Duffy JF, Wang W, Czeisler CA, Shea SA. Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci Transl Med 2012;4:129ra43.
71. Leproult R, Holmback U, Van Cauter E. Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes 2014;63:1860-9.
72. Morris CJ, Yang JN, Garcia JI, Myers S, Bozzi I, Wang W, Buxton OM, Shea SA, Scheer FA. Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans. Proc Natl Acad Sci USA 2015;112:E2225-34.
73. Dibner C, Schibler U. Circadian timing of metabolism in animal models and humans. J Intern Med 2015;277:513-27.
74. Perelis M, Ramsey KM, Bass J. The molecular clock as a metabolic rheostat. Diabetes Obes Metab 2015;17 Suppl 1:99-105.
75. Stephan FK. The "other" circadian system: food as a Zeitgeber. J Biol Rhythms 2002;17:284-92.
76. Mistlberger RE. Food-anticipatory circadian rhythms: concepts and methods. Eur J Neurosci 2009;30:1718-29.
77. Krieger DT, Hauser H, Krey LC. Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science 1977;197:398-9.
78. Challet E, Mendoza J, Dardente H, Pevet P. Neurogenetics of food anticipation. Eur J Neurosci 2009;30:1676-87.
79. Storch KF, Weitz CJ. Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock. Proc Natl Acad Sci USA 2009;106:6808-13.
80. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 2000;14:2950-61.
81. Johnston JD. Physiological responses to food intake throughout the day. Nutr Res Rev 2014;27:107-18.
82. Asher G, Sassone-Corsi P. Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell 2015;161:84-92.
83. Arble DM, Bass J, Laposky AD, Vitaterna MH, Turek FW. Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring) 2009;17:2100-2.
84. Sherman H, Genzer Y, Cohen R, Chapnik N, Madar Z, Froy O. Timed high-fat diet resets circadian metabolism and prevents obesity. FASEB J 2012;26:3493-502.
85. Chaix A, Zarrinpar A, Miu P, Panda S. Time-restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metab 2014;20:991-1005.
86. Gill S, Le HD, Melkani GC, Panda S. Time-restricted feeding attenuates age-related cardiac decline in Drosophila. Science 2015;347:1265-9.
87. Jakubowicz D, Barnea M, Wainstein J, Froy O. High caloric intake at breakfast vs. dinner differentially influences weight loss of overweight and obese women. Obesity (Silver Spring) 2013;21:2504-12.
88. Jakubowicz D,Wainstein J, Ahren B, Bar-Dayan Y, Landau Z, Rabinovitz HR, Froy O. High-energy breakfast with low-energy dinner decreases overall daily hyperglycaemia in type 2 diabetic patients: a randomised clinical trial. Diabetologia 2015;58:912-9.
89. Garaulet M, Gomez-Abellan P, Alburquerque-Bejar JJ, Lee YC, Ordovas JM, Scheer FA. Timing of food intake predicts weight loss effectiveness. Int J Obes (Lond) 2013;37:604-11.
90. Morris CJ, Garcia JI, Myers S, Yang JN, Trienekens N, Scheer FA. The human circadian system has a dominating role in causing the morning/evening difference in diet-induced thermogenesis. Obesity (Silver Spring) 2015;23:2053-8.
91. Romon M, Edme JL, Boulenguez C, Lescroart JL, Frimat P. Circadian variation of diet-induced thermogenesis. Am J Clin Nutr 1993;57:476-80.
92. Weststrate JA, Weys PJ, Poortvliet EJ, Deurenberg P, Hautvast JG. Diurnal variation in postabsorptive resting metabolic rate and diet-induced thermogenesis. Am J Clin Nutr 1989;50:908-14.
93. Loboda A, Kraft WK, Fine B, Joseph J, Nebozhyn M, Zhang C, He Y, Yang X, Wright C, Morris M, et al. Diurnal variation of the human adipose transcriptome and the link to metabolic disease. BMC Med Genomics 2009;2:7.
94. Otway DT, Mantele S, Bretschneider S, Wright J, Trayhurn P, Skene DJ, Robertson MD, Johnston JD. Rhythmic diurnal gene expression in human adipose tissue from individuals who are lean, overweight, and type 2 diabetic. Diabetes 2011;60:1577-81.
95. Brown SA, Fleury-Olela F, Nagoshi E, Hauser C, Juge C, Meier CA, Chicheportiche R, Dayer JM, Albrecht U, Schibler U. The period length of fibroblast circadian gene expression varies widely among human individuals. PLoS Biol 2005;3:e338.
96. Hasan S, Santhi N, Lazar AS, Slak A, Lo J, von Schantz M, Archer SN, Johnston JD, Dijk DJ. Assessment of circadian rhythms in humans: comparison of real-time fibroblast reporter imaging with plasma melatonin. FASEB J 2012;26:2414-23.