Pinealectomy interferes with the circadian clock genes expression in white adipose tissue

Journal of Pineal Research

Volumn 58, Issue 3, 2015, Pages 251-261

  De Farias, Talita Da Silva Mendes ^a   De Oliveira, Ariclécio Cunha ^a   Andreotti, Sandra ^a   Do Amaral, Fernanda Gaspar ^b   Chimin, Patrícia ^a   De Proença, André Ricardo Alves ^a   Torres Leal, Francisco Leonardo ^a   Sertié, Rogério Antonio Laurato ^a   Campana, Amanda Baron ^a   Lopes, Andressa Bolsoni ^a   De Souza, Arnaldo Henrique ^a   Cipolla Neto, José ^a   Lima, Fabio Bessa ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

adipose tissue; clock genes; melatonin; metabolism; pinealectomy

Indexed keywords

ADENOSINE TRIPHOSPHATE CITRATE SYNTHASE; ADIPOCYTOKINE; FATTY ACID SYNTHASE; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; LEPTIN; LYASE; MALATE DEHYDROGENASE (DECARBOXYLATING); MELATONIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRIACYLGLYCEROL; CIRCADIAN RHYTHM SIGNALING PROTEIN;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CLOCK GENE; CONTROLLED STUDY; CRY1 GENE; CYTOKINE PRODUCTION; ENZYME ACTIVITY; EPIDIDYMIS FAT; FATTY ACID SYNTHESIS; GENE; GENE EXPRESSION; LIPID METABOLISM; LIPOGENESIS; MALE; METABOLIC REGULATION; NONHUMAN; PER2 GENE; PINEALECTOMY; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; WHITE ADIPOSE TISSUE; WISTAR RAT; ANIMAL; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PINEAL BODY; SURGERY;

ADIPOSE TISSUE, WHITE; ANIMALS; CIRCADIAN RHYTHM; GENE EXPRESSION; MALE; PERIOD CIRCADIAN PROTEINS; PINEAL GLAND; RATS; RATS, WISTAR;

EID: 84924717555     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12211     Document Type: Article

References (62)

1. Johnston JD, Frost G, Otway DT,. Adipose tissue, adipocytes and the circadian timing system. Obes Rev 2009; 10 (Suppl 2): 52-60.
2. Cardinali DP, Cano P, Jiménez-Ortega V, et al. Melatonin and the metabolic syndrome: physiopathologic and therapeutical implications. Neuroendocrinology 2011; 93: 133-142.
3. Garaulet M, Madrid JA,. Chronobiology, genetics and metabolic syndrome. Curr Opin Lipidol 2009; 20: 127-134.
4. Bartness TJ, Goldman BD,. Mammalian pineal melatonin: a clock for all seasons. Experientia 1989; 45: 939-945.
5. Wang XS, Armstrong ME, Cairns BJ, et al. Shift work and chronic disease: the epidemiological evidence. Occup Med (Lond) 2011; 61: 78-89.
6. di Lorenzo L, de Pergola G, Zocchetti C, et al. Effect of shift work on body mass index: results of a study performed in 319 glucose-tolerant men working in a Southern Italian industry. Int J Obes Relat Metab Disord 2003; 27: 1353-1358.
7. Coomans CP, van den Berg SA, Houben T, et al. Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity. FASEB J 2013; 27: 1721-1732.
8. Bartness TJ, Wade GN,. Photoperiodic control of seasonal body weight cycles in hamsters. Neurosci Biobehav Rev 1985; 9: 599-612.
9. Rasmussen DD, Mitton DR, Larsen SA, et al. Aging-dependent changes in the effect of daily melatonin supplementation on rat metabolic and behavioral responses. J Pineal Res 2001; 31: 89-94.
10. Prunet-Marcassus B, Desbazeille M, Bros A, et al. Melatonin reduces body weight gain in Sprague Dawley rats with diet-induced obesity. Endocrinology 2003; 144: 5347-5352.
11. Zanquetta MM, Corrêa-Giannella ML, Monteiro MB, et al. Body weight, metabolism and clock genes. Diabetol Metab Syndr 2010; 2: 53.
12. Cipolla-Neto J, Amaral FG, Afeche SC, et al. Melatonin, energy metabolism, and obesity: a review. J Pineal Res 2014; 56: 371-381.
13. Alonso-Vale MI, Anhê GF, Borges-Silva C, et al. Pinealectomy alters adipose tissue adaptability to fasting in rats. Metabolism 2004; 53: 500-506.
14. Arendt J, Skene DJ,. Melatonin as a chronobiotic. Sleep Med Rev 2005; 9: 25-39.
15. Archer SN, Laing EE, Möller-Levet CS, et al. Mistimed sleep disrupts circadian regulation of the human transcriptome. Proc Natl Acad Sci USA 2014; 111: E682-E691.
16. Gõmez-Abellán P, Hernández-Morante JJ, Luján JA, et al. Clock genes are implicated in the human metabolic syndrome. Int J Obes (Lond) 2008; 32: 121-128.
17. 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.
18. Froy O,. Metabolism and circadian rhythms-implications for obesity. Endocr Rev 2010; 31: 1-24.
19. Takahashi JS, Hong HK, Ko CH, et al. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 2008; 9: 764-775.
20. Preitner N, Damiola F, Lopez-Molina L, et al. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002; 110: 251-260.
21. Ueda HR, Chen W, Adachi A, et al. A transcription factor response element for gene expression during circadian night. Nature 2002; 418: 534-539.
22. Poulsen L, Siersbæk M, Mandrup S,. PPARs: fatty acid sensors controlling metabolism. Semin Cell Dev Biol 2012; 23: 631-639.
23. Schupp M, Lazar MA,. Endogenous ligands for nuclear receptors: digging deeper. J Biol Chem 2010; 285: 40409-40415.
24. Yang X, Downes M, Yu RT, et al. Nuclear receptor expression links the circadian clock to metabolism. Cell 2006; 126: 801-810.
25. Tontonoz P, Hu E, Spiegelman BM,. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 1994; 79: 1147-1156.
26. Ribon V, Johnson JH, Camp HS, et al. Thiazolidinediones and insulin resistance: peroxisome proliferatoractivated receptor gamma activation stimulates expression of the CAP gene. Proc Natl Acad Sci USA 1998; 95: 14751-14756.
27. Rodbell M,. Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis. J Biol Chem 1964; 239: 375-380.
28. Digirolamo M,. Measurements of glucose conversion to its metabolites. Methods Mol Biol 2001; 155: 181-192.
29. Zanuto R, Siqueira-Filho MA, Caperuto LC, et al. Melatonin improves insulin sensitivity independently of weight loss in old obese rats. J Pineal Res 2013; 55: 156-165.
30. Mendes C, Lopes AM, Amaral FG, et al. Adaptations of the aging animal to exercise: role of daily supplementation with melatonin. J Pineal Res 2013; 55: 229-239.
31. Green CB, Takahashi JS, Bass J,. The meter of metabolism. Cell 2008; 134: 728-742.
32. Reiter RJ,. The pineal gland and seasonal reproductive adjustments. Int J Biometeorol 1975; 19: 282-288.
33. Barrett P, Bolborea M,. Molecular pathways involved in seasonal body weight and reproductive responses governed by melatonin. J Pineal Res 2012; 52: 376-388.
34. Alonso-Vale MI, Andreotti S, Mukai PY, et al. Melatonin and the circadian entrainment of metabolic and hormonal activities in primary isolated adipocytes. J Pineal Res 2008; 45: 422-429.
35. Vriend J, Reiter RJ,. Melatonin feedback on clock genes: a theory involving the proteasome. J Pineal Res 2015; 58: 1-11.
36. Lima FB, Matsushita DH, Hell NS, et al. The regulation of insulin action in isolated adipocytes. Role of the periodicity of food intake, time of day and melatonin. Braz J Med Biol Res 1994; 27: 995-1000.
37. Lima FB, Machado UF, Bartol I, et al. Pinealectomy causes glucose intolerance and decreases adipose cell responsiveness to insulin in rats. Am J Physiol 1998; 275: E934-E941.
38. Alonso-Vale MI, Borges-Silva CN, Anhê GF, et al. Light/dark cycle-dependent metabolic changes in adipose tissue of pinealectomized rats. Horm Metab Res 2004; 36: 474-479.
39. Alonso-Vale MI, Andreotti S, Peres SB, et al. Melatonin enhances leptin expression by rat adipocytes in the presence of insulin. Am J Physiol Endocrinol Metab 2005; 288: E805-E812.
40. Jiménez-Aranda A, Fernández-Vázquez G, Campos D, et al. Melatonin induces browning of inguinal white adipose tissue in Zucker diabetic fatty rats. J Pineal Res 2013; 55: 416-423.
41. Rudic RD, McNamara P, Curtis AM, et al. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol 2004; 2: e377.
42. Zhang EE, Liu Y, Dentin R, et al. Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat Med 2010; 16: 1152-1156.
43. Andrews JL, Zhang X, McCarthy JJ, et al. CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function. Proc Natl Acad Sci USA 2010; 107: 19090-19095.
44. 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.
45. Grimaldi B, Bellet MM, Katada S, et al. PER2 controls lipid metabolism by direct regulation of PPARγ. Cell Metab 2010; 12: 509-520.
46. Delezie J, Dumont S, Dardente H, et al. The nuclear receptor REV-ERBα is required for the daily balance of carbohydrate and lipid metabolism. FASEB J 2012; 26: 3321-3335.
47. Solt LA, Wang Y, Banerjee S, et al. Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 2012; 485: 62-68.
48. Baggs JE, Price TS, Ditacchio L, et al. Network features of the mammalian circadian clock. PLoS Biol 2009; 7: e1000052.
49. Inoue I, Shinoda Y, Ikeda M, et al. CLOCK/BMAL1 is involved in lipid metabolism via transactivation of the peroxisome proliferator-activated receptor (PPAR) response element. J Atheroscler Thromb 2005; 12: 169-174.
50. Chen L, Yang G,. PPARs integrate the mammalian clock and energy metabolism. PPAR Res 2014; 2014: 653017.
51. Yang G, Jia Z, Aoyagi T, et al. Systemic Pparγ deletion impairs circadian rhythms of behavior and metabolism. PLoS One 2012; 7: e38117.
52. Rosen ED, Walkey CJ, Puigserver P, et al. Transcriptional regulation of adipogenesis. Genes Dev 2000; 14: 1293-1307.
53. He W, Barak Y, Hevener A, et al. Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 2003; 100: 15712-15717.
54. Duan SZ, Ivashchenko CY, Whitesall SE, et al. Hypotension, lipodystrophy, and insulin resistance in generalized PPARgamma-deficient mice rescued from embryonic lethality. J Clin Invest 2007; 117: 812-822.
55. 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.
56. Oishi K, Shirai H, Ishida N,. CLOCK is involved in the circadian transactivation of peroxisome-proliferator-activated receptor alpha (PPARalpha) in mice. Biochem J 2005; 386: 575-581.
57. Damiola F, le Minh N, Preitner N, et al. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 2000; 14: 2950-2961.
58. Stokkan KA, Yamazaki S, Tei H, et al. Entrainment of the circadian clock in the liver by feeding. Science 2001; 291: 490-493.
59. Bechtold DA,. Energy-responsive timekeeping. J Genet 2008; 87: 447-458.
60. Kalsbeek A, la Fleur S, van Heijningen C, et al. Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J Neurosci 2004; 24: 7604-7613.
61. Pocai A, Obici S, Schwartz GJ, et al. A brain-liver circuit regulates glucose homeostasis. Cell Metab 2005; 1: 53-61.
62. Cailotto C, van Heijningen C, van der Vliet J, et al. Daily rhythms in metabolic liver enzymes and plasma glucose require a balance in the autonomic output to the liver. Endocrinology 2008; 149: 1914-1925.