Association of weight regain with specific methylation levels in the NPY and POMC promoters in leukocytes of obese men: A translational study

Regulatory Peptides

Volumn 186, Issue , 2013, Pages 1-6

  Crujeiras, Ana B ^a,b,e   Campion, Javier ^c,e   Díaz Lagares, Angel ^a,d   Milagro, Fermin I ^c,e   Goyenechea, Estíbaliz ^c,e   Abete, Itziar ^c,e   Casanueva, Felipe F ^b,e   Martínez, J Alfredo ^c,e  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

^d Fundación Pública Galega Medicina Xenómica FPGMX   (Spain)

^e CIBER Fisiopatología de la Obesidad y la Nutrición   (Spain)

Author keywords

Blood cells; Epigenetic biomarkers; Ghrelin; Leptin; Obesity

Indexed keywords

GHRELIN; LEPTIN; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DIET THERAPY; DNA METHYLATION; EPIGENETICS; GENETIC ASSOCIATION; HORMONE BLOOD LEVEL; HUMAN; LEUKOCYTE; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NPY GENE; OBESITY; POMC GENE; PRIORITY JOURNAL; PROMOTER REGION; RISK ASSESSMENT; WEIGHT GAIN; WEIGHT REDUCTION; WEIGHT REGAIN;

BLOOD CELLS; EPIGENETIC BIOMARKERS; GHRELIN; LEPTIN; OBESITY;

CPG ISLANDS; DNA METHYLATION; GHRELIN; HUMANS; LEPTIN; LEUKOCYTES; MALE; NEUROPEPTIDE Y; OBESITY; PRO-OPIOMELANOCORTIN; PROMOTER REGIONS, GENETIC; RECEPTORS, LEPTIN; WEIGHT GAIN;

EID: 84881006702     PISSN: 01670115     EISSN: 18731686     Source Type: Journal    
DOI: 10.1016/j.regpep.2013.06.012     Document Type: Article

References (56)

1. Napolitano A., Miller S.R., Murgatroyd P.R., Delafont B., Brooke A., Elkhawad M., Tan C.Y., Virtue S., Vidal-Puig A., Nunez D.J. Prediction of weight loss and regain following dietary, lifestyle, and pharmacologic intervention. Clin Pharmacol Ther 2012, 91:1027-1034.
2. Maclean P.S., Bergouignan A., Cornier M.A., Jackman M.R. Biology's response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol 2011, 301:R581-R600.
3. MacLean P.S., Higgins J.A., Jackman M.R., Johnson G.C., Fleming-Elder B.K., Wyatt H.R., Melanson E.L., Hill J.O. Peripheral metabolic responses to prolonged weight reduction that promote rapid, efficient regain in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 2006, 290:R1577-R1588.
4. Sumithran P., Prendergast L.A., Delbridge E., Purcell K., Shulkes A., Kriketos A., Proietto J. Long-term persistence of hormonal adaptations to weight loss. N Engl J Med 2011, 365:1597-1604.
5. Crujeiras A.B., Goyenechea E., Abete I., Lage M., Carreira M.C., Martinez J.A., Casanueva F.F. Weight regain after a diet-induced loss is predicted by higher baseline leptin and lower ghrelin plasma levels. J Clin Endocrinol Metab 2010, 95:5037-5044.
6. Erez G., Tirosh A., Rudich A., Meiner V., Schwarzfuchs D., Sharon N., Shpitzen S., Bluher M., Stumvoll M., Thiery J., Fiedler G.M., Friedlander Y., Leiterstdorf E., Shai I. Phenotypic and genetic variation in leptin as determinants of weight regain. Int J Obes (Lond) 2011, 35:785-792.
7. Goyenechea E., Crujeiras A.B., Abete I., Martinez J.A. Expression of two inflammation-related genes (RIPK3 and RNF216) in mononuclear cells is associated with weight-loss regain in obese subjects. J Nutrigenet Nutrigenomics 2009, 2:78-84.
8. Goyenechea E., Parra M.Dolores, Martinez J.Alfredo Weight regain after slimming induced by an energy-restricted diet depends on interleukin-6 and peroxisome-proliferator-activated-receptor-gamma2 gene polymorphisms. Br J Nutr 2006, 96:965-972.
9. Goyenechea E., Parra D., Crujeiras A.B., Abete I., Martinez J.A. A nutrigenomic inflammation-related PBMC-based approach to predict the weight-loss regain in obese subjects. Ann Nutr Metab 2009, 54:43-51.
10. Campion J., Milagro F., Martinez J.A. Epigenetics and obesity. Prog Mol Biol Transl Sci 2010, 94:291-347.
11. Martinez J.A., Cordero P., Campion J., Milagro F.I. Interplay of early-life nutritional programming on obesity, inflammation and epigenetic outcomes. Proc Nutr Soc 2012, 1-8.
12. Portela A., Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010, 28:1057-1068.
13. Rodriguez-Paredes M., Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med 2011, 17:330-339.
14. Bouchard L., Rabasa-Lhoret R., Faraj M., Lavoie M.E., Mill J., Perusse L., Vohl M.C. Differential epigenomic and transcriptomic responses in subcutaneous adipose tissue between low and high responders to caloric restriction. Am J Clin Nutr 2010, 91:309-320.
15. Campion J., Milagro F.I., Goyenechea E., Martinez J.A. TNF-alpha promoter methylation as a predictive biomarker for weight-loss response. Obesity (Silver Spring) 2009, 17:1293-1297.
16. Milagro F.I., Campion J., Cordero P., Goyenechea E., Gomez-Uriz A.M., Abete I., Zulet M.A., Martinez J.A. A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J 2011, 25:1378-1389.
17. Cordero P., Campion J., Milagro F.I., Goyenechea E., Steemburgo T., Javierre B.M., Martinez J.A. Leptin and TNF-alpha promoter methylation levels measured by MSP could predict the response to a low-calorie diet. J Physiol Biochem 2011, 67:463-470.
18. Zhao J., Goldberg J., Vaccarino V. Promoter methylation of serotonin transporter gene is associated with obesity measures: a monozygotic twin study. Int J Obes (Lond) 2013, 37:140-145.
19. Levin B.E. The drive to regain is mainly in the brain. Am J Physiol Regul Integr Comp Physiol 2004, 287:R1297-R1300.
20. Berthoud H.R., Morrison C. The brain, appetite, and obesity. Annu Rev Psychol 2008, 59:55-92.
21. Plagemann A., Harder T., Brunn M., Harder A., Roepke K., Wittrock-Staar M., Ziska T., Schellong K., Rodekamp E., Melchior K., Dudenhausen J.W. Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome. J Physiol 2009, 587:4963-4976.
22. Stevens A., Begum G., Cook A., Connor K., Rumball C., Oliver M., Challis J., Bloomfield F., White A. Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. Endocrinology 2010, 151:3652-3664.
23. Paternain L., Batlle M.A., De la Garza A.L., Milagro F.I., Martinez J.A., Campion J. Transcriptomic and epigenetic changes in the hypothalamus are involved in an increased susceptibility to a high-fat-sucrose diet in prenatally stressed female rats. Neuroendocrinology 2012, 96:249-260.
24. Palou M., Pico C., McKay J.A., Sanchez J., Priego T., Mathers J.C., Palou A. Protective effects of leptin during the suckling period against later obesity may be associated with changes in promoter methylation of the hypothalamic pro-opiomelanocortin gene. Br J Nutr 2011, 106:769-778.
25. Terry M.B., Delgado-Cruzata L., Vin-Raviv N., Wu H.C., Santella R.M. DNA methylation in white blood cells: association with risk factors in epidemiologic studies. Epigenetics 2011, 6:828-837.
26. Zhang F.F., Cardarelli R., Carroll J., Zhang S., Fulda K.G., Gonzalez K., Vishwanatha J.K., Morabia A., Santella R.M. Physical activity and global genomic DNA methylation in a cancer-free population. Epigenetics 2011, 6:293-299.
27. Zhang F.F., Morabia A., Carroll J., Gonzalez K., Fulda K., Kaur M., Vishwanatha J.K., Santella R.M., Cardarelli R. Dietary patterns are associated with levels of global genomic DNA methylation in a cancer-free population. J Nutr 2011, 141:1165-1171.
28. Zhang F.F., Cardarelli R., Carroll J., Fulda K.G., Kaur M., Gonzalez K., Vishwanatha J.K., Santella R.M., Morabia A. Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood. Epigenetics 2011, 6:623-629.
29. D'Addario C., Dell'osso B., Palazzo M.C., Benatti B., Lietti L., Cattaneo E., Galimberti D., Fenoglio C., Cortini F., Scarpini E., Arosio B., Di Francesco A., Di Benedetto M., Romualdi P., Candeletti S., Mari D., Bergamaschini L., Bresolin N., Maccarrone M., Altamura A.C. Selective DNA methylation of BDNF promoter in bipolar disorder: differences among patients with BDI and BDII. Neuropsychopharmacology 2012, 37:1647-1655.
30. Bollati V., Galimberti D., Pergoli L., Dalla Valle E., Barretta F., Cortini F., Scarpini E., Bertazzi P.A., Baccarelli A. DNA methylation in repetitive elements and Alzheimer disease. Brain Behav Immun 2011, 25:1078-1083.
31. Ehrlich S., Weiss D., Burghardt R., Infante-Duarte C., Brockhaus S., Muschler M.A., Bleich S., Lehmkuhl U., Frieling H. Promoter specific DNA methylation and gene expression of POMC in acutely underweight and recovered patients with anorexia nervosa. J Psychiatr Res 2010, 44:827-833.
32. Cai M., Tian J., Zhao G.H., Luo W., Zhang B.R. Study of methylation levels of parkin gene promoter in Parkinson's disease patients. Int J Neurosci 2011, 121:497-502.
33. Crujeiras A.B., Parra D., Goyenechea E., Abete I., Martinez J.A. Tachyphylaxis effects on postprandial oxidative stress and mitochondrial-related gene expression in overweight subjects after a period of energy restriction. Eur J Nutr 2009, 48:341-347.
34. Crujeiras A.B., Diaz-Lagares A., Goyenechea E., Abete I., Amil-Diz M., Lage M., Carreira M.C., Casanueva F.F., Martinez J.A. Evaluación de la utilidad pronóstica del cociente leptina/ghrelina para identificar a los pacientes capaces de mantener el peso perdido tras una dieta hipocalórica. Endocrinol Nutr 2011, 58:80.
35. Garcia-Carpizo V., Ruiz-Llorente L., Fraga M., Aranda A. The growing role of gene methylation on endocrine function. J Mol Endocrinol 2011, 47:R75-R89.
36. Ilhan A., Rasul S., Dimitrov A., Handisurya A., Gartner W., Baumgartner-Parzer S., Wagner L., Kautzky-Willer A., Base W. Plasma neuropeptide Y levels differ in distinct diabetic conditions. Neuropeptides 2010, 44:485-489.
37. Kalra S.P., Dube M.G., Pu S., Xu B., Horvath T.L., Kalra P.S. Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr Rev 1999, 20:68-100.
38. Kos K., Harte A.L., James S., Snead D.R., O'Hare J.P., McTernan P.G., Kumar S. Secretion of neuropeptide Y in human adipose tissue and its role in maintenance of adipose tissue mass. Am J Physiol Endocrinol Metab 2007, 293:E1335-E1340.
39. Singer K., Morris D.L., Oatmen K.E., Wang T., DelProposto J., Mergian T., Cho K.W., Lumeng C.N. Neuropeptide Y is produced by adipose tissue macrophages and regulates obesity-induced inflammation. PLoS One 2013, 8:e57929.
40. Hussain T., Al-Daghri N.M., Al-Attas O.S., Draz H.M., Abd Al-Rahman S.H., Yakout S.M. Plasma neuropeptide Y levels relate cigarette smoking and smoking cessation to body weight regulation. Regul Pept 2012, 176:22-27.
41. Li N.F., Yao X.G., Zhu J., Yang J., Liu K.J., Wang Y.C., Wang X.L., Zu F.Y. Higher levels of plasma TNF-alpha and neuropeptide Y in hypertensive patients with obstructive sleep apnea syndrome. Clin Exp Hypertens 2010, 32:54-60.
42. Uriz J., Gines P., Ortega R., Jimenez W., Cardenas A., Calahorra B., Sort P., Fernandez J., Bataller R., Arroyo V., Rivera F., Rodes J. Increased plasma levels of neuropeptide Y in hepatorenal syndrome. J Hepatol 2002, 36:349-355.
43. Byun C.J., Seo J., Jo S.A., Park Y.J., Klug M., Rehli M., Park M.H., Jo I. DNA methylation of the 5'-untranslated region at +298 and +351 represses BACE1 expression in mouse BV-2 microglial cells. Biochem Biophys Res Commun 2012, 417:387-392.
44. Marchi M., Lisi S., Curcio M., Barbuti S., Piaggi P., Ceccarini G., Nannipieri M., Anselmino M., Di Salvo C., Vitti P., Pinchera A., Santini F., Maffei M. Human leptin tissue distribution, but not weight loss-dependent change in expression, is associated with methylation of its promoter. Epigenetics 2012, 6:1198-1206.
45. Quandt K., Frech K., Karas H., Wingender E., Werner T. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 1995, 23:4878-4884.
46. Burnett E., Christensen J., Tattersall P. A consensus DNA recognition motif for two KDWK transcription factors identifies flexible-length, CpG-methylation sensitive cognate binding sites in the majority of human promoters. J Mol Biol 2001, 314:1029-1039.
47. Adkins R.M., Somes G., Morrison J.C., Hill J.B., Watson E.M., Magann E.F., Krushkal J. Association of birth weight with polymorphisms in the IGF2, H19, and IGF2R genes. Pediatr Res 2010, 68:429-434.
48. St-Pierre J., Hivert M.F., Perron P., Poirier P., Guay S.P., Brisson D., Bouchard L. IGF2 DNA methylation is a modulator of newborn's fetal growth and development. Epigenetics 2012, 7.
49. Payne V.A., Au W.S., Lowe C.E., Rahman S.M., Friedman J.E., O'Rahilly S., Rochford J.J. C/EBP transcription factors regulate SREBP1c gene expression during adipogenesis. Biochem J 2009, 425:215-223.
50. Martínez-Gonzánelez M.A., Sánchez-villegas A., Faulin-Fajardo J. Bioestadística amigable 2010, Díaz de Santos, Madrid.
51. Heyn H., Carmona F.J., Gomez A., Ferreira H.J., Bell J.T., Sayols S., Ward K., Stefansson O.A., Moran S., Sandoval J., Eyfjord J.E., Spector T.D., Esteller M. DNA methylation profiling in breast cancer discordant identical twins identifies DOK7 as novel epigenetic biomarker. Carcinogenesis 2013, 34:102-108.
52. Moleres A., Rendo-Urteaga T., Zulet M.A., Marcos A., Campoy C., Garagorri J.M., Martinez J.A., Azcona-Sanjulian M.C., Marti A. Obesity Susceptibility loci on body mass index and weight loss in Spanish adolescents after a lifestyle intervention. J Pediatr 2012, 161:466-470.
53. Plourde M., Vohl M.C., Bellis C., Carless M., Dyer T., Dolley G., Marette A., Despres J.P., Bouchard C., Blangero J., Perusse L. A variant in the LRRFIP1 gene is associated with adiposity and inflammation. Obesity (Silver Spring) 2013, 21:185-192.
54. Burdge G.C., Hoile S.P., Lillycrop K.A. Epigenetics: are there implications for personalised nutrition?. Curr Opin Clin Nutr Metab Care 2012, 15:442-447.
55. Vucetic Z., Carlin J.L., Totoki K., Reyes T.M. Epigenetic dysregulation of the dopamine system in diet-induced obesity. J Neurochem 2012, 120:891-898.
56. Egecioglu E., Skibicka K.P., Hansson C., Alvarez-Crespo M., Friberg P.A., Jerlhag E., Engel J.A., Dickson S.L. Hedonic and incentive signals for body weight control. Rev Endocr Metab Disord 2011, 12:141-151.