CLOCK, PER2 and BMAL1 DNA methylation: Association with obesity and metabolic syndrome characteristics and monounsaturated fat intake

Chronobiology International

Volumn 29, Issue 9, 2012, Pages 1180-1194

  Milagro, Fermín I ^a   Gómez Abellán, Purificación ^b   Campión, Javier ^a   Martínez, J Alfredo ^a   Ordovás, Jose M ^c,d,e   Garaulet, Marta ^b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

^c TUFTS UNIVERSITY   (United States)

^d CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^e IMDEA FOOD INSTITUTE   (Spain)

Author keywords

Biomarker; Cytosine methylation; Epigenetics; MassARRAY; MUFA

Indexed keywords

ARNTL PROTEIN, HUMAN; CIRCADIAN RHYTHM SIGNALING PROTEIN; CLOCK PROTEIN, HUMAN; DNA; PER2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR ARNTL; TRANSCRIPTION FACTOR CLOCK;

ADULT; ARTICLE; BIOLOGICAL RHYTHM; CASE CONTROL STUDY; CPG ISLAND; DNA METHYLATION; FAT INTAKE; FEMALE; GENETIC MARKER; GENETICS; HUMAN; METABOLIC SYNDROME X; MIDDLE AGED; MOLECULAR GENETICS; MORBID OBESITY; NUCLEOTIDE SEQUENCE; OBESITY; WEIGHT REDUCTION;

ADULT; ARNTL TRANSCRIPTION FACTORS; BASE SEQUENCE; BIOLOGICAL CLOCKS; CASE-CONTROL STUDIES; CLOCK PROTEINS; CPG ISLANDS; DIETARY FATS; DNA; DNA METHYLATION; FEMALE; GENETIC MARKERS; HUMANS; METABOLIC SYNDROME X; MIDDLE AGED; MOLECULAR SEQUENCE DATA; OBESITY; OBESITY, MORBID; OVERWEIGHT; PERIOD CIRCADIAN PROTEINS; WEIGHT REDUCTION PROGRAMS;

EID: 84867286546     PISSN: 07420528     EISSN: 15256073     Source Type: Journal    
DOI: 10.3109/07420528.2012.719967     Document Type: Article

References (46)

1. Alberti KG, Zimmet P, Shaw J, IDF Epidemiology Task Force Consensus Group. (2005). The metabolic syndrome: A new worldwide definition. Lancet 366:1059-1062.
2. Bollati V, Baccarelli A, Sartori S, Tarantini L, Motta V, Rota F, Costa G. (2010). Epigenetic effects of shiftwork on blood DNA methylation. Chronobiol. Int. 27:1093-1104.
3. Bouchard L, Rabasa-Lhoret R, Faraj M, Lavoie ME, Mill J, Pérusse L, Vohl MC. (2010). Differential epigenomic and transcriptomic responses in subcutaneous adipose tissue between low and high responders to caloric restriction. Am. J. Clin. Nutr. 91:309-320.
4. Campión J, Milagro F, Martínez JA. (2010). Epigenetics and obesity. Prog. Mol. Biol. Transl. Sci. 94:291-347.
5. Cardinali DP, Cano P, Jiménez-Ortega V, Esquifino AI. (2011). Melatonin and the metabolic syndrome: Physiopathologic and therapeutical implications. Neuroendocrinology 93:133-142.
6. Ceccarelli V, Racanicchi S, Martelli MP, Nocentini G, Fettucciari K, Riccardi C, Marconi P, Di Nardo P, Grignani F, Binaglia L, Vecchini A. (2011). Eicosapentaenoic acid demethylates a single CpG that mediates expression of tumor suppressor CCAAT/enhancerbinding protein delta in U937 leukemia cells. J. Biol. Chem. 286:27092-27102.
7. Corbalán MD, Morales EM, Canteras M, Espallardo A, Hernández T, Garaulet M. (2009). Effectiveness of cognitive-behavioral therapy based on the Mediterranean diet for the treatment of obesity. Nutrition 25:861-869.
8. Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, Aspelund T, Eiriksdottir G, Harris TB, Launer L, Gudnason V, Fallin MD. (2010). Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci. Transl. Med. 2:49ra67.
9. Fick LJ, Fick GH, Belsham DD. (2011). Palmitate alters the rhythmic expression of molecular clock genes and orexigenic neuropeptide Y mRNA levels within immortalized, hypothalamic neurons. Biochem. Biophys. Res. Commun. 413:414-449.
10. Gangwisch JE. (2009). Epidemiological evidence for the links between sleep, circadian rhythms and metabolism. Obes. Rev. 10:37-45.
11. Garaulet M, Corbalán MD, Madrid JA, Morales E, Baraza JC, Lee YC, Ordovas JM. (2010a). CLOCK gene is implicated in weight reduction in obese patients participating in a dietary programme based on the Mediterranean diet. Int. J. Obes. 34:516-523.
12. Garaulet M, Corbalán-Tutau MD, Madrid JA, Baraza JC, Parnell LD, Lee YC, Ordovas JM. (2010b). PERIOD2 variants are associated with abdominal obesity, psycho-behavioral factors, and attrition in the dietary treatment of obesity. J. Am. Diet. Assoc. 110:917-921.
13. Garaulet M, Madrid JA. (2010). Chronobiological aspects of nutrition, metabolic syndrome and obesity. Adv. Drug Deliv. Rev. 62:967-978.
14. Garaulet M, Lee YC, Shen J, Parnell LD, Arnett DK, Tsai MY, Lai CQ, Ordovas JM (2009). CLOCK genetic variation and metabolic syndrome risk: Modulation by monounsaturated fatty acids. Am. J. Clin. Nutr. 90:1466-1475.
15. Garaulet M, Ortega FB, Ruiz JR, Rey-López JP, Béghin L, Manios Y, Cuenca-García M, Plada M, Diethelm K, Kafatos A, Molnár D, Al- Tahan J, Moreno LA. (2011a). Short sleep duration is associated with increased obesity markers in European adolescents: Effect of physical activity and dietary habits. The HELENA study. Int. J. Obes. 35:1308-1317.
16. Garaulet M, Sánchez-Moreno C, Smith CE, Lee YC, Nicolás F, Ordovás JM. (2011b). Ghrelin, sleep reduction and evening preference: Relationships to CLOCK 3111 T/C SNP and weight loss. PLoS One 6:e17435.
17. Godfrey KM, Sheppard A, Gluckman PD, Lillycrop KA, Burdge GC, McLean C, Rodford J, Slater-Jefferies JL, Garratt E, Crozier SR, Emerald BS, Gale CR, Inskip HM, Cooper C, Hanson MA. (2011). Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes 60:1528-1534.
18. Gómez-Abellán P, Hernández-Morante JJ, Luján JA, Madrid JA, Garaulet M. (2008). Clock genes are implicated in the human metabolic syndrome. Int. J. Obes. 32:121-128.
19. Gómez-Santos C, Gómez-Abellán P, Madrid JA, Hernández-Morante JJ, Lujan JA, Ordovas JM, Garaulet M. (2009). Circadian rhythm of clock genes in human adipose explants. Obesity 17:1481-1485.
20. Havel RJ, Eder HA, Bragdon JH. (1955). The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 34:1345-1353.
21. Hernandez-Morante JJ, Gomez-Santos C, Margareto J, Formiguera X, Martínez CM, González R, Martínez-Augustín O, Madrid JA, Ordovas JM, Garaulet M. (2011). Influence of menopause on adipose tissue clock gene genotype and its relationship with metabolic syndrome in morbidly obese women. Age (in press)
22. Horne JA, Ostberg O. (1976). A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 4:97-110.
23. Kiec-Wilk B, Sliwa A, Mikolajczyk M, Malecki MT, Mathers JC. (2011). The CpG island methylation regulated expression of endothelial proangiogenic genes in response to β-carotene and arachidonic acid. Nutr. Cancer 63:1053-1063.
24. Korkmaz A, Sanchez-Barcelo EJ, Tan DX, Reiter RJ. (2009). Role of melatonin in the epigenetic regulation of breast cancer. Breast Cancer Res. Treat. 115:13-27.
25. Kotronoulas G, Stamatakis A, Stylianopoulou F. (2009). Hormones, hormonal agents, and neuropeptides involved in the neuroendocrine regulation of sleep in humans. Hormones 8:232-248.
26. Kulkarni A, Dangat K, Kale A, Sable P, Chavan-Gautam P, Joshi S. (2011). Effects of altered maternal folic acid, vitamin B12 and docosahexaenoic acid on placental global DNA methylation patterns in Wistar rats. PLoS One 6:e17706.
27. Lillycrop KA, Burdge GC. (2011). Epigenetic changes in early life and future risk of obesity. Int. J. Obes. 35:72-83.
28. Lomba A, Martínez JA, García-Díaz DF, Paternain L, Marti A, Campión J, Milagro FI. (2010). Weight gain induced by an isocaloric pair-fed high fat diet: A nutriepigenetic study on FASN and NDUFB6 gene promoters. Mol. Genet. Metab. 101:273-278.
29. Manenschijn L, van Kruysbergen RG, de Jong FH, Koper JW, van Rossum EF. (2011). Shift work at young age is associated with elevated long-term cortisol levels and body mass index. J. Clin. Endocrinol. Metab. 96:E1862-E1865.
30. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C,Mo S, Vitaterna MH, Lopez JP, Philipson LH, Bradfield CA, Crosby SD, JeBailey L, Wang X, Takahashi JS, Bass J. (2010). Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466:627-631.
31. McAllister EJ, Dhurandhar NV, Keith SW, Aronne LJ, Barger J, Baskin M, Benca RM, Biggio J, Boggiano MM, Eisenmann JC, Elobeid M, Fontaine KR, Gluckman P, Hanlon EC, Katzmarzyk P, Pietrobelli A, Redden DT, Ruden DM, Wang C, Waterland RA, Wright SM, Allison DB. (2009). Ten putative contributors to the obesity epidemic. Crit. Rev. Food Sci. Nutr. 49:868-913.
32. Milagro FI, Campión J, Cordero P, Goyenechea E, Gómez-Uriz AM, Abete I, Zulet MA, Martínez JA. (2011). A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J. 25:1378-1389.
33. Moreiras O, Carvajal A, Cabrera L, Cuadrado C. (2009). Tablas de composición de alimentos. 13rd ed. Madrid: Ediciones Pirámide, 83 pp
34. Perez-Llamas F, Garaulet M, Herrero F, Palma JT, Perez de Heredia F, Marin R, Zamora S. (2004). Multivalent informatics application for studies of the nutritional status of the population. Assessment of food intake. Nutr. Hosp. 19:160-166.
35. Portaluppi F, Smolensky MH, Touitou Y. (2010). Ethics and methods for biological rhythm research on animals and human beings. Chronobiol. Int. 27:1911-1929.
36. Rudic RD, McNamara P, Curtis AM, Boston RC, Panda S, Hogenesch JB, Fitzgerald GA. (2004). BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2:e377.
37. Serra-Majem L, Aranceta J, SENC Working Group on Nutritional Objectives for the Spanish Population. (2001). Spanish Society of Community Nutrition. Nutritional objectives for the Spanish population. Consensus from the Spanish Society of Community Nutrition. Public Health Nutr. 4:1409-1413.
38. Sheward WJ, Maywood ES, French KL, Horn JM, Hastings MH, Seckl JR, Holmes MC, Harmar AJ. (2007). Entrainment to feeding but not to light: Circadian phenotype of VPAC2 receptor-null mice. J. Neurosci. 27:4351-4358.
39. Shih MC, Yeh KT, Tang KP, Chen JC, Chang JG. (2006). Promoter methylation in circadian genes of endometrial cancers detected by methylation-specific PCR. Mol. Carcinog. 45:732-740.
40. Shimba S, Ogawa T, Hitosugi S, Ichihashi Y, Nakadaira Y, Kobayashi M, Tezuka M, Kosuge Y, Ishige K, Ito Y, Komiyama K, Okamatsu-Ogura Y, Kimura K, Saito M. (2011). Deficient of a clock gene, brain and muscle Arnt-like protein-1 (BMAL1), induces dyslipidemia and ectopic fat formation. PLoS One 6:e25231.
41. Sookoian S, Gemma C, Gianotti TF, Burgueno A, Castano G, Pirola CJ. (2008). Genetic variants of Clock transcription factor are associated with individual susceptibility to obesity. Am. J. Clin. Nutr. 87:1606-1615.
42. Suter M, Bocock P, Showalter L, Hu M, Shope C, McKnight R, Grove K, Lane R, Aagaard-Tillery K. (2011). Epigenomics: Maternal high-fat diet exposure in utero disrupts peripheral circadian gene expression in nonhuman primates. FASEB J. 25:714-726.
43. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, Eckel RH, Takahashi JS, Bass J. (2005). Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308:1043-1045.
44. Wadhwa PD, Buss C, Entringer S, Swanson JM. (2009). Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin. Reprod. Med. 27:358-368.
45. Warnick GR, Benderson J, Albers JJ. (1982). Dextran sulfate-Mg21 precipitation procedure for quantitation of high-densitylipoprotein cholesterol. Clin. Chem. 28:1379-1388.
46. Zhu Y, Stevens RG, Hoffman AE, Tjonneland A, Vogel UB, Zheng T, Hansen J. (2011). Epigenetic impact of long-term shiftwork: Pilot evidence from circadian genes and whole-genome methylation analysis. Chronobiol. Int. 28:852-861.