Circadian rhythms in adipose tissue: An update

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 14, Issue 6, 2011, Pages 554-561

  Gimble, Jeffrey M ^a   Sutton, Gregory M ^a   Ptitsyn, Andrey A ^b   Floyd, Z Elizabeth ^a   Bunnell, Bruce A ^c  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

adipose; circadian; clock; entrainer; metabolism

Indexed keywords

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; CIRCADIAN RHYTHM; DROSOPHILA; GENE; GENE DELETION; HIBERNATION; HUMAN; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; LIPID DIET; LIPID METABOLISM; NONHUMAN; OBESITY; REVIEW;

ADIPOCYTES; ADIPOSE TISSUE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CIRCADIAN RHYTHM; DIET, HIGH-FAT; DROSOPHILA; GENE DELETION; HUMANS; MICE; MODELS, ANIMAL; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

MAMMALIA; MURINAE;

EID: 80054987998     PISSN: 13631950     EISSN: 14736519     Source Type: Journal    
DOI: 10.1097/MCO.0b013e32834ad94b     Document Type: Review

References (93)

1. Asher G, Schibler U. Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab 2011; 13:125-137.
2. Yu W, Hardin PE. Circadian oscillators of Drosophila and mammals. J Cell Sci 2006; 119:4793-4795. (Pubitemid 46017791)
3. Takahashi JS, Hong HK, Ko CH, McDearmon EL. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 2008; 9:764-775.
4. Maury E, Ramsey KM, Bass J. Circadian rhythms and metabolic syndrome: from experimental genetics to human disease. Circ Res 2010; 106:447-462.
5. Froy O. Metabolism and circadian rhythms: implications for obesity. Endocr Rev 2010; 31:1-24.
6. Froy O. The circadian clock and metabolism. Clin Sci (Lond) 2011; 120:65-72.
7. Garaulet M, Ordovas JM, Madrid JA. The chronobiology, etiology and pathophysiology of obesity. Int J Obes (Lond) 2010; 34:1667-1683.
8. Kalsbeek A, Bruinstroop E, Yi CX, et al. Hypothalamic control of energy metabolism via the autonomic nervous system. Ann N Y Acad Sci 2010; 1212:114-129.
9. Kawai M, Rosen CJ. PPARgamma: a circadian transcription factor in adipogenesis and osteogenesis. Nat Rev Endocrinol 2010; 6:629-636.
10. Schug TT, Li X. Sirtuin 1 in lipid metabolism and obesity. Ann Med 2011; 43:198-211.
11. Zanquetta MM, Correa-Giannella ML, Monteiro MB, Villares SM. Body weight, metabolism and clock genes. Diabetol Metab Syndr 2010; 2:53.
12. Kojetin DJ, Burris TP. A role for Rev-erbalpha ligands in regulation of adipogenesis. Curr Pharm Des 2011; 17:320-324.
13. Gimble JM, Sutton GM, Bunnell BA, et al. Prospective influences of circadian clocks in adipose tissue and metabolism. Nat Rev Endocrinol 2011; 7:98-107.
14. Bray MS, Young ME. Regulation of fatty acid metabolism by cell autonomous circadian clocks: time to fatten up on information? J Biol Chem 2011; 286:11883-11889.
15. Bray MS, Tsai JY, Villegas-Montoya C, et al. Time-of-day-dependent dietary fat consumption influences multiple cardiometabolic syndrome parameters in mice. Int J Obes (Lond) 2010; 34:1589-1598.
16. Kaneko K, Yamada T, Tsukita S, et al. Obesity alters circadian expressions of molecular clock genes in the brainstem. Brain Res 2009; 1263:58-68.
17. Ando H, Kumazaki M, Motosugi Y, et al. Impairment of peripheral circadian clocks precedes metabolic abnormalities in ob/ob mice. Endocrinology 2011; 152:1347-1354.
18. Hsieh MC, Yang SC, Tseng HL, et al. Abnormal expressions of circadianclock and circadian clock-controlled genes in the livers and kidneys of longterm, high-fat-diet-treated mice. Int J Obes (Lond) 2010; 34:227-239.
19. Kohsaka A, Laposky AD, Ramsey KM, et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 2007; 6:414-421. (Pubitemid 350011997)
20. Ando H, Ushijima K, Yanagihara H, et al. Clock gene expression in the liver and adipose tissues of nonobese type 2 diabetic Goto-Kakizaki rats. Clin Exp Hypertens 2009; 31:201-207.
21. Sukumaran S, Xue B, Jusko WJ, et al. Circadian variations in gene expression in rat abdominal adipose tissue and relationship to physiology. Physiol Genomics 2010; 42A:141-152.
22. Zvonic S, Ptitsyn AA, Conrad SA, et al. Characterization of peripheral circadian clocks in adipose tissues. Diabetes 2006; 55:962-970. (Pubitemid 44100170)
23. Loboda A, Kraft WK, Fine B, et al. Diurnal variation of the human adipose transcriptome and the link to metabolic disease. BMC Med Genomics 2009; 2:7.
24. Um JH, Pendergast JS, Springer DA, et al. AMPK regulates circadian rhythms in a tissue-and isoform-specific manner. PLoS One 2011; 6:e18450.
25. Shimba S, Ishii N, Ohta Y, et al. Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci USA 2005; 102:12071-12076. (Pubitemid 41291130)
26. Shi X, Shi W, Li Q, et al. A glucocorticoid-induced leucine-zipper protein, GILZ, inhibits adipogenesis of mesenchymal cells. EMBO Rep 2003; 4:374-380. (Pubitemid 36622002)
27. Gimble JM, Ptitsyn AA, Goh BC, et al. Delta sleep-inducing peptide and glucocorticoid-induced leucine zipper: potential links between circadian mechanisms and obesity? Obes Rev 2009; 10 (Suppl 2):46-51.
28. Gilbert MR, Douris N, Tongjai S, Green CB. Nocturnin expression is induced by fasting in the white adipose tissue of restricted fed mice. PLoS One 2011; 6:e17051.
29. Green CB, Douris N, Kojima S, et al. Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proc Natl Acad Sci USA 2007; 104:9888-9893. (Pubitemid 47175361)
30. Sonoda J, Mehl IR, Chong LW, et al. PGC-1beta controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis. Proc Natl Acad Sci USA 2007; 104:5223-5228. (Pubitemid 47186203)
31. Liu C, Li S, Liu T, et al. Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 2007; 447:477-481. (Pubitemid 46816732)
32. Lemberger T, Saladin R, Vazquez M, et al. Expression of the peroxisome proliferator-activated receptor alpha gene is stimulated by stress and follows a diurnal rhythm. J Biol Chem 1996; 271:1764-1769. (Pubitemid 26028664)
33. Canaple L, Rambaud J, Dkhissi-Benyahya O, et al. 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; 20:1715-1727. (Pubitemid 44148079)
34. Goh BC, Wu X, Evans AE, et al. Food entrainment of circadian gene expression altered in PPARα-/-brown fat and heart. Biochem Biophys Res Commun 2007; 360:828-833. (Pubitemid 47077395)
35. Kumar N, Solt LA, Wang Y, et al. Regulation of adipogenesis by natural and synthetic REV-ERB ligands. Endocrinology 2010; 151:3015-3025.
36. Yin L, Wu N, Lazar MA. Nuclear receptor Rev-erbalpha: a heme receptor that coordinates circadian rhythm and metabolism. Nucl Recept Signal 2010; 8:e001.
37. Lau P, Fitzsimmons RL, Raichur S, et al. The orphan nuclear receptor, RORalpha, regulates gene expression that controls lipid metabolism: staggerer (SG/SG) mice are resistant to diet-induced obesity. J Biol Chem 2008; 283:18411-18421.
38. Ohoka N, Kato S, Takahashi Y, et al. The orphan nuclear receptor RORalpha restrains adipocyte differentiation through a reduction of C/EBPbeta activity and perilipin gene expression. Mol Endocrinol 2009; 23:759-771.
39. Tontonoz P, Kim JB, Graves RA, Spiegelman BM. ADD1: a novel helix-loophelix transcription factor associated with adipocyte determination and differentiation. Mol Cell Biol 1993; 13:4753-4759.
40. Brewer M, Lange D, Baler R, Anzulovich A. SREBP-1 as a transcriptional integrator of circadian and nutritional cues in the liver. J Biol Rhythms 2005; 20:195-205. (Pubitemid 40646940)
41. Matsumoto E, Ishihara A, Tamai S, et al. Time of day and nutrients in feeding govern daily expression rhythms of the gene for sterol regulatory elementbinding protein (SREBP)-1 in the mouse liver. J Biol Chem 2010; 285:33028-33036.
42. Ramsey KM, Yoshino J, BraceCS, et al. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 2009; 324:651-654.
43. Um JH, Yang S, Yamazaki S, et al. Activation of 5′-AMP-activated kinase with diabetes drug metformin induces casein kinase Iepsilon (CKIepsilon)-dependent degradation of clock protein mPer2. J Biol Chem 2007; 282:20794-20798. (Pubitemid 47099893)
44. Kondratov RV, Kondratova AA, Gorbacheva VY, et al. Early aging and agerelated pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev 2006; 20:1868-1873. (Pubitemid 44088348)
45. Shi S, Hida A, McGuinness OP, et al. Circadian clock gene Bmal1 is not essential; functional replacement with its paralog, Bmal2. Curr Biol 2010; 20:316-321.
46. Grimaldi B, Bellet MM, Katada S, et al. PER2 controls lipid metabolism by direct regulation of PPARgamma. Cell Metab 2010; 12:509-520.
47. Dallmann R, Weaver DR. Altered body mass regulation in male mPeriod mutant mice on high-fat diet. Chronobiol Int 2010; 27:1317-1328.
48. Li R, Yue J, Zhang Y, et al. CLOCK/BMAL1 regulates human nocturnin transcription through binding to the E-box of nocturnin promoter. Mol Cell Biochem 2008; 317:169-177.
49. Kawai M, Delany AM, Green CB, et al. Nocturnin suppresses igf1 expression in bone by targeting the 3′ untranslated region of igf1 mRNA. Endocrinology 2010; 151:4861-4870.
50. Kawai M, Green CB, Lecka-Czernik B, et al. A circadian-regulated gene, Nocturnin, promotes adipogenesis by stimulating PPAR-gamma nuclear translocation. Proc Natl Acad Sci USA 2010; 107:10508-10513.
51. Chiu HK, Qian K, Ogimoto K, et al. Mice lacking hepatic lipase are lean and protected against diet-induced obesity and hepatic steatosis. Endocrinology 2010; 151:993-1001.
52. Hoy AJ, Bruce CR, Turpin SM, et al. Adipose triglyceride lipase-null mice are resistant to high-fat diet-induced insulin resistance despite reduced energy expenditure and ectopic lipid accumulation. Endocrinology 2011; 152:48-58.
53. Hou L, Lu C, Huang Y, et al. Effect of hyperlipidemia on the expression of circadian genes in apolipoprotein E knock-out atherosclerotic mice. Lipids Health Dis 2009; 8:60.
54. He Y, Wu X, Khan RS, et al. IL-15 receptor deletion results in circadian changes of locomotor and metabolic activity. J Mol Neurosci 2010; 41:315-321.
55. Oishi K. Disrupted light-dark cycle induces obesity with hyperglycemia in genetically intact animals. Neuro Endocrinol Lett 2009; 30:458-461.
56. Wideman CH, Murphy HM. Constant light induces alterations in melatonin levels, food intake, feed efficiency, visceral adiposity, and circadian rhythms in rats. Nutr Neurosci 2009; 12:233-240.
57. Glad CA, Kitchen EE, Russ GC, et al. Reverse feeding suppresses the activity of the GH axis in rats and induces a preobesogenic state. Endocrinology 2011; 152:869-882.
58. Salgado-Delgado R, Angeles-Castellanos M, Saderi N, et al. Food intake during the normal activity phase prevents obesity and circadian desynchrony in a rat model of night work. Endocrinology 2010; 151:1019-1029.
59. Hasek BE, Stewart LK, Henagan TM, et al. Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states. Am J Physiol Regul Integr Comp Physiol 2010; 299:R728-R739.
60. Sutton GM, Centanni AV, Butler AA. Protein malnutrition during pregnancy in C57BL/6J mice results in offspring with altered circadian physiology before obesity. Endocrinology 2010; 151:1570-1580.
61. Nelson CJ, Otis JP, Carey HV. A role for nuclear receptors in mammalian hibernation. J Physiol 2009; 587:1863-1870.
62. Leitner C, Bartness TJ. Distributed forebrain sites mediate melatonin-induced short-day responses in Siberian hamsters. Endocrinology 2010; 151:3133-3140.
63. Golub V. Stopping the clock: neobiosis as a predecessor of mammalian hibernation and possible key to the abolition of aging. Rejuvenation Res 2010; 13:343-346.
64. Stawski C, Geiser F. Fat and fed: frequent use of summer torpor in a subtropical bat. Naturwissenschaften 2010; 97:29-35.
65. Wang Y, Solt LA, Burris TP. Regulation of FGF21 expression and secretion by retinoic acid receptor-related orphan receptor alpha. J Biol Chem 2010; 285:15668-15673.
66. Inagaki T, Dutchak P, Zhao G, et al. Endocrine regulation of the fasting response by PPARα-mediated induction of fibroblast growth factor 21. Cell Metab 2007; 5:415-425. (Pubitemid 46825496)
67. Badman MK, Pissios P, Kennedy AR, et al. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab 2007; 5:426-437. (Pubitemid 46825495)
68. Kharitonenkov A, Shiyanova TL, Koester A, et al. FGF-21 as a novel metabolic regulator. J Clin Invest 2005; 115:1627-1635. (Pubitemid 40814671)
69. Estall JL, Ruas JL, Choi CS, et al. PGC-1alpha negatively regulates hepatic FGF21 expression by modulating the heme/Rev-Erb(alpha) axis. Proc Natl Acad Sci USA 2009; 106:22510-22515.
70. Hondares E, Rosell M, Gonzalez FJ, et al. Hepatic FGF21 expression is induced at birth via PPARalpha in response to milk intake and contributes to thermogenic activation of neonatal brown fat. Cell Metab 2010; 11:206-212.
71. Gupta AK, Cornelissen G, Greenway FL, et al. Abnormalities in circadian blood pressure variability and endothelial function: pragmatic markers for adverse cardiometabolic profiles in asymptomatic obese adults. Cardiovasc Diabetol 2010; 9:58.
72. Gupta AK, Greenway FL, Cornelissen G, et al. Prediabetes is associated with abnormal circadian blood pressure variability. J Hum Hypertens 2008; 22:627-633.
73. Masaki T, Anan F, Yoshimatsu H. Visceral fat accumulation is associated with circadian blood pressure in Japanese patients with impaired glucose tolerance. Diabetes Care 2011; 34:e32.
74. Jeong E, Youn BS, Kim DW, et al. Circadian rhythm of serum vaspin in healthy male volunteers: relation to meals. J Clin Endocrinol Metab 2010; 95:1869-1875.
75. Scheer FA, Chan JL, Fargnoli J, et al. Day/night variations of high-molecularweight adiponectin and lipocalin-2 in healthy men studied under fed and fasted conditions. Diabetologia 2010; 53:2401-2405.
76. Suneja M,Murry DJ, Stokes JB, Lim VS. Hormonal regulation of energy-protein homeostasis in hemodialysis patients: an anorexigenic profile that may predispose to adverse cardiovascular outcomes. Am J Physiol Endocrinol Metab 2011; 300:E55-E64.
77. Hill EE, Eisenmann JC, Holmes ME, Heelan KA. Morning cortisol is not associated with truncal fatness or resting blood pressure in children: cross-sectional and 1-2 year follow-up analyses. J Pediatr Endocrinol Metab 2010; 23:1031-1037.
78. Garaulet M, Corbalan MD, Madrid JA, et al. 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; 34:516-523.
79. Garaulet M, Corbalan-Tutau MD, Madrid JA, et al. PERIOD2 variants are associated with abdominal obesity, psycho-behavioral factors, and attrition in the dietary treatment of obesity. J Am Diet Assoc 2010; 110:917-921.
80. Garaulet M, Lee YC, Shen J, et al. Genetic variants in human CLOCK associate with total energy intake and cytokine sleep factors in overweight subjects (GOLDN population). Eur J Hum Genet 2010; 18:364-369.
81. Garaulet M, Ordovas JM, Gomez-Abellan P, et al. An approximation to the temporal order in endogenous circadian rhythms of genes implicated in human adipose tissue metabolism. J Cell Physiol 2010; 226:2075-2080.
82. Gomez-Abellan P, Gomez-Santos C, Madrid JA, et al. Circadian expression of adiponectin and its receptors in human adipose tissue. Endocrinology 2010; 151:115-122.
83. Otway DT, Mantele S, Bretschneider S, et al. Rhythmic diurnal gene expression in human adipose tissue from individuals who are lean, overweight, and have type 2 diabetes. Diabetes 2011; 60:1577-1581.
84. Ando H, Yanagihara H, Hayashi Y, et al. Rhythmic mRNA expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 2005; 146:5631-5636. (Pubitemid 41653080)
85. Fujikawa K, Takahashi A, Nishimura A, et al. Characteristics of genes upregulated and down-regulated after 24 h starvation in the head of Drosophila. Gene 2009; 446:11-17.
86. DiAngelo JR, Bland ML, Bambina S, et al. The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc Natl Acad Sci USA 2009; 106:20853-20858.
87. Benito J, Hoxha V, Lama C, et al. The circadian output gene takeout is regulated by Pdp1epsilon. Proc Natl Acad Sci USA 2010; 107:2544-2549.
88. Sarov-Blat L, So WV, Liu L, Rosbash M. The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell 2000; 101:647-656.
89. Beaver LM, Hooven LA, Butcher SM, et al. Circadian clock regulates response to pesticides in Drosophila via conserved Pdp1 pathway. Toxicol Sci 2010; 115:513-520.
90. Carhan A, Tang K, Shirras CA, et al. Loss of angiotensin-converting enzymerelated (ACER) peptidase disrupts night-time sleep in adult Drosophila melanogaster. J Exp Biol 2011; 214:680-686.
91. Kuo TH, Pike DH, Beizaeipour Z, Williams JA. Sleep triggered by an immune response in Drosophila is regulated by the circadian clock and requires the NFkappaB Relish. BMC Neurosci 2010; 11:17.
92. Helenius IT, Krupinski T, Turnbull DW, et al. Elevated CO2 suppresses specific Drosophila innate immune responses and resistance to bacterial infection. Proc Natl Acad Sci USA 2009; 106:18710-18715.
93. Sell H, Eckel J. Adipose tissue inflammation: novel insight into the role of macrophages and lymphocytes. Curr Opin Clin Nutr Metab Care 2010; 13:366-370.