Promoter methylation of glucocorticoid receptor gene is associated with subclinical atherosclerosis: A monozygotic twin study

Atherosclerosis

Volumn 242, Issue 1, 2015, Pages 71-76

  Zhao, Jinying ^a   An, Qiang ^a   Goldberg, Jack ^b,c   Quyyumi, Arshed A ^d   Vaccarino, Viola ^d,e  

^a TULANE UNIVERSITY   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e EMORY UNIVERSITY   (United States)

Author keywords

DNA methylation; Monozygotic twins; NR3C1; Subclinical atherosclerosis

Indexed keywords

BISULFITE; GENOMIC DNA; GLUCOCORTICOID RECEPTOR; GLUCOSE; GLUCOSE BLOOD LEVEL; LIPID;

ADULT; ARTICLE; ATHEROSCLEROSIS; BODY MASS; BRACHIAL ARTERY; CONTROLLED STUDY; CPG ISLAND; DEPRESSION; DILATATION; DNA METHYLATION; ENVIRONMENTAL FACTOR; EXON; FAMILY; FLOW MEDIATED DILATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GLUCOSE BLOOD LEVEL; HEREDITY; HUMAN; INTRAVASCULAR ULTRASOUND; LEUKOCYTE; MAJOR CLINICAL STUDY; MALE; METHYLATION; MIDDLE AGED; MONOZYGOTIC TWINS; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; SMOKING; VIET NAM; AGED; ANALYSIS; ARTERIAL STIFFNESS; ASYMPTOMATIC DISEASE; BLOOD; BLOOD PRESSURE; EPIDEMIOLOGY; GENETICS; MOLECULAR GENETICS; MOTOR ACTIVITY; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; REGISTER; RISK FACTOR; TWINS; UNITED STATES; VASODILATATION;

AGED; ASYMPTOMATIC DISEASES; ATHEROSCLEROSIS; BASE SEQUENCE; BLOOD GLUCOSE; BLOOD PRESSURE; BODY MASS INDEX; BRACHIAL ARTERY; CONFOUNDING FACTORS (EPIDEMIOLOGY); CPG ISLANDS; DEPRESSION; DISEASES IN TWINS; DNA METHYLATION; EXONS; HUMANS; LIPIDS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MOTOR ACTIVITY; PROMOTER REGIONS, GENETIC; RECEPTORS, GLUCOCORTICOID; REGISTRIES; RISK FACTORS; SMOKING; TWINS, MONOZYGOTIC; UNITED STATES; VASCULAR STIFFNESS; VASODILATION;

EID: 84936994102     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2015.07.007     Document Type: Article

References (48)

1. Singh R.B., Mengi S.A., Xu Y.J., Arneja A.S., Dhalla N.S. Pathogenesis of atherosclerosis: a multifactorial process. Exp. Clin. Cardiol. 2002, 7:40-53.
2. Lund G., Andersson L., Lauria M., Lindholm M., Fraga M.F., Villar-Garea A., Ballestar E., Esteller M., Zaina S. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J.Biol. Chem. 2004, 279:29147-29154.
3. Zaina S., Heyn H., Carmona F.J., Varol N., Sayols S., Condom E., Ramirez-Ruz J., Gomez A., Goncalves I., Moran S., Esteller M. ADNA methylation map of human atherosclerosis. Circ. Cardiovasc. Genet. 2014, 7(5):692-700.
4. Zhao J., Goldberg J., Bremner J.D., Vaccarino V. Global DNA methylation is associated with insulin resistance: a monozygotic twin study. Diabetes 2012, 61:542-546.
5. 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(1):140-145.
6. Zhao J., Goldberg J., Bremner J.D., Vaccarino V. Association between promoter methylation of serotonin transporter gene and depressive symptoms: a monozygotic twin study. Psychosom. Med. 2013, 75:523-529.
7. Corretti M.C., Anderson T.J., Benjamin E.J., Celermajer D., Charbonneau F., Creager M.A., Deanfield J., Drexler H., Gerhard-Herman M., Herrington D., Vallance P., Vita J., Vogel R. International Brachial Artery Reactivity Task F. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J.Am. Coll. Cardiol. 2002, 39:257-265.
8. Vita J.A., Keaney J.F. Endothelial function: a barometer for cardiovascular risk?. Circulation 2002, 106:640-642.
9. Shechter M., Shechter A., Koren-Morag N., Feinberg M.S., Hiersch L. Usefulness of brachial artery flow-mediated dilation to predict long-term cardiovascular events in subjects without heart disease. Am. J. Cardiol. 2014, 113:162-167.
10. Widlansky M.E., Gokce N., Keaney J.F., Vita J.A. The clinical implications of endothelial dysfunction. J.Am. Coll. Cardiol. 2003, 42:1149-1160.
11. Lerman A., Zeiher A.M. Endothelial function: cardiac events. Circulation 2005, 111:363-368.
12. Bonetti P.O., Lerman L.O., Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler. Thromb. Vasc. Biol. 2003, 23:168-175.
13. Flammer A.J., Anderson T., Celermajer D.S., Creager M.A., Deanfield J., Ganz P., Hamburg N.M., Luscher T.F., Shechter M., Taddei S., Vita J.A., Lerman A. The assessment of endothelial function: from research into clinical practice. Circulation 2012, 126:753-767.
14. Hollenberg S.M., Weinberger C., Ong E.S., Cerelli G., Oro A., Lebo R., Thompson E.B., Rosenfeld M.G., Evans R.M. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 1985, 318:635-641.
15. Kadmiel M., Cidlowski J.A. Glucocorticoid receptor signaling in health and disease. Trends Pharmacol. Sci. 2013, 34:518-530.
16. Daxinger L., Whitelaw E. Transgenerational epigenetic inheritance: more questions than answers. Genome Res. 2010, 20:1623-1628.
17. Zhao J., Cheema F.A., Reddy U., Bremner J.D., Su S., Goldberg J., Snieder H., Vaccarino V. Heritability of flow-mediated dilation: a twin study. J.Thromb. Haemost. 2007, 5:2386-2392.
18. Bohacek J., Mansuy I.M. Epigenetic inheritance of disease and disease risk. Neuropsychopharmacology 2013, 38:220-236.
19. Goldberg J., Curran B., Vitek M.E., Henderson W.G., Boyko E.J. The Vietnam era twin registry. Twin Res. 2002, 5:476-481.
20. Vaccarino V., Khan D., Votaw J., Faber T., Veledar E., Jones D.P., Goldberg J., Raggi P., Quyyumi A.A., Bremner J.D. Inflammation is related to coronary flow reserve detected by positron emission tomography in asymptomatic male twins. J.Am. Coll. Cardiol. 2011, 57:1271-1279.
21. Hill J.M., Zalos G., Halcox J.P., Schenke W.H., Waclawiw M.A., Quyyumi A.A., Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N.Engl. J. Med. 2003, 348:593-600.
22. Richardson M.T., Ainsworth B.E., Wu H.C., Jacobs D.R., Leon A.S. Ability of the Atherosclerosis Risk in Communities (ARIC)/Baecke Questionnaire to assess leisure-time physical activity. Int. J. Epidemiol. 1995, 24:685-693.
23. Beck A.T., Steer R.A., Brown G.K. Manual for the Beck Depression Inventory-II 1996, Psychological Corporation, San Antonio, TX.
24. Vaccarino V., Goldberg J., Rooks C., Shah A.J., Veledar E., Faber T.L., Votaw J.R., Forsberg C.W., Bremner J.D. Post-traumatic stress disorder and incidence of coronary heart disease: a twin study. J.Am. Coll. Cardiol. 2013, 62:970-978.
25. Turner J.D., Alt S.R., Cao L., Vernocchi S., Trifonova S., Battello N., Muller C.P. Transcriptional control of the glucocorticoid receptor: CpG islands, epigenetics and more. Biochem. Pharmacol. 2010, 80:1860-1868.
26. Martin-Blanco A., Ferrer M., Soler J., Salazar J., Vega D., Andion O., Sanchez-Mora C., Arranz M.J., Ribases M., Feliu-Soler A., Perez V., Pascual J.C. Association between methylation of the glucocorticoid receptor gene, childhood maltreatment, and clinical severity in borderline personality disorder. J.Psychiatric Res. 2014, 57:34-40.
27. Klengel T., Pape J., Binder E.B., Mehta D. The role of DNA methylation in stress-related psychiatric disorders. Neuropharmacology 2014, 80:115-132.
28. Perroud N., Paoloni-Giacobino A., Prada P., Olie E., Salzmann A., Nicastro R., Guillaume S., Mouthon D., Stouder C., Dieben K., Huguelet P., Courtet P., Malafosse A. Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma. Transl. Psychiatry 2011, 1:e59.
29. Gluckman P.D., Hanson M.A., Buklijas T., Low F.M., Beedle A.S. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat. Rev. Endocrinol. 2009, 5:401-408.
30. Carlin J.B., Gurrin L.C., Sterne J.A., Morley R., Dwyer T. Regression models for twin studies: a critical review. Int. J. Epidemiol. 2005, 34:1089-1099.
31. Dempster E.L., Pidsley R., Schalkwyk L.C., Owens S., Georgiades A., Kane F., Kalidindi S., Picchioni M., Kravariti E., Toulopoulou T., Murray R.M., Mill J. Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum. Mol. Genet. 2011, 20:4786-4796.
32. Rakyan V.K., Beyan H., Down T.A., Hawa M.I., Maslau S., Aden D., Daunay A., Busato F., Mein C.A., Manfras B., Dias K.R., Bell C.G., Tost J., Boehm B.O., Beck S., Leslie R.D. Identification of type 1 diabetes-associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet. 2011, 7:e1002300.
33. Javierre B.M., Fernandez A.F., Richter J., Al-Shahrour F., Martin-Subero J.I., Rodriguez-Ubreva J., Berdasco M., Fraga M.F., O'Hanlon T.P., Rider L.G., Jacinto F.V., Lopez-Longo F.J., Dopazo J., Forn M., Peinado M.A., Carreno L., Sawalha A.H., Harley J.B., Siebert R., Esteller M., Miller F.W., Ballestar E. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res. 2010, 20:170-179.
34. Kaminsky Z.A., Tang T., Wang S.C., Ptak C., Oh G.H., Wong A.H., Feldcamp L.A., Virtanen C., Halfvarson J., Tysk C., McRae A.F., Visscher P.M., Montgomery G.W., Gottesman I.I., Martin N.G., Petronis A. DNA methylation profiles in monozygotic and dizygotic twins. Nat. Genet. 2009, 41:240-245.
35. Manolio T.A., Collins F.S., Cox N.J., Goldstein D.B., Hindorff L.A., Hunter D.J., McCarthy M.I., Ramos E.M., Cardon L.R., Chakravarti A., Cho J.H., Guttmacher A.E., Kong A., Kruglyak L., Mardis E., Rotimi C.N., Slatkin M., Valle D., Whittemore A.S., Boehnke M., Clark A.G., Eichler E.E., Gibson G., Haines J.L., Mackay T.F., McCarroll S.A., Visscher P.M. Finding the missing heritability of complex diseases. Nature 2009, 461:747-753.
36. Frigola J., Song J., Stirzaker C., Hinshelwood R.A., Peinado M.A., Clark S.J. Epigenetic remodeling in colorectal cancer results in coordinate gene suppression across an entire chromosome band. Nat. Genet. 2006, 38:540-549.
37. Novak P., Jensen T., Oshiro M.M., Watts G.S., Kim C.J., Futscher B.W. Agglomerative epigenetic aberrations are a common event in human breast cancer. Cancer Res. 2008, 68:8616-8625.
38. Walker B.R. Glucocorticoids and cardiovascular disease. Eur. J. Endocrinol. 2007, 157:545-559.
39. Rosmond R., Bjorntorp P. The hypothalamic-pituitary-adrenal axis activity as a predictor of cardiovascular disease, type 2 diabetes and stroke. J.Intern. Med. 2000, 247:188-197.
40. Rosmond R., Chagnon Y.C., Holm G., Chagnon M., Perusse L., Lindell K., Carlsson B., Bouchard C., Bjorntorp P. Aglucocorticoid receptor gene marker is associated with abdominal obesity, leptin, and dysregulation of the hypothalamic-pituitary-adrenal axis. Obes. Res. 2000, 8:211-218.
41. Laryea G., Schutz G., Muglia L.J. Disrupting hypothalamic glucocorticoid receptors causes HPA axis hyperactivity and excess adiposity. Mol. Endocrinol. 2013, 27:1655-1665.
42. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
43. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009, 12:342-348.
44. Pitzalis C., Pipitone N., Perretti M. Regulation of leukocyte-endothelial interactions by glucocorticoids. Ann. N. Y. Acad. Sci. 2002, 966:108-118.
45. Menke A., Binder E.B. Epigenetic alterations in depression and antidepressant treatment. Dialogues Clin. Neurosci. 2014, 16:395-404.
46. Probst A.V., Dunleavy E., Almouzni G. Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell. Biol. 2009, 10:192-206.
47. Rutten B.P., Mill J. Epigenetic mediation of environmental influences in major psychotic disorders. Schizophr. Bull. 2009, 35:1045-1056.
48. Sun C., Burgner D.P., Ponsonby A.L., Saffery R., Huang R.C., Vuillermin P.J., Cheung M., Craig J.M. Effects of early-life environment and epigenetics on cardiovascular disease risk in children: highlighting the role of twin studies. Pediatr. Res. 2013, 73:523-530.