The effects of omega-3 polyunsaturated fatty acids and genetic variants on methylation levels of the interleukin-6 gene promoter

Molecular Nutrition and Food Research

Volumn 60, Issue 2, 2016, Pages 410-419

  Ma, Yiyi ^a,b   Smith, Caren E ^a   Lai, Chao Qiang ^a   Irvin, Marguerite R ^c   Parnell, Laurence D ^a   Lee, Yu Chi ^a   Pham, Lucia D ^a   Aslibekyan, Stella ^c   Claas, Steven A ^c   Tsai, Michael Y ^d   Borecki, Ingrid B ^e   Kabagambe, Edmond K ^f   Ordovás, José M ^a,g,h   Absher, Devin M ⁱ   Arnett, Donna K ^c  

^a TUFTS UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f VANDERBILT UNIVERSITY   (United States)

^g CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^h IMDEA FOOD INSTITUTE   (Spain)

ⁱ HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

Author keywords

DNA methylation; Gene by environment interaction; Genetic variant; Interleukin 6; n 3 polyunsaturated fatty acids

Indexed keywords

IL6 PROTEIN, HUMAN; INTERLEUKIN 6; OMEGA 3 FATTY ACID;

ADULT; BLOOD; CPG ISLAND; DNA METHYLATION; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; MALE; MIDDLE AGED; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; CPG ISLANDS; DNA METHYLATION; FATTY ACIDS, OMEGA-3; FEMALE; HUMANS; INTERLEUKIN-6; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC;

EID: 84947968852     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500436     Document Type: Article

References (41)

1. Farzaneh-Far, R., Harris, W. S., Garg, S., Na, B. et al., Inverse association of erythrocyte n-3 fatty acid levels with inflammatory biomarkers in patients with stable coronary artery disease: The Heart and Soul Study. Atherosclerosis 2009, 205, 538-543.
2. Trebble, T., Arden, N. K., Stroud, M. A., Wootton, S. A. et al., Inhibition of tumour necrosis factor-alpha and interleukin 6 production by mononuclear cells following dietary fish-oil supplementation in healthy men and response to antioxidant co-supplementation. Br. J. Nutr. 2003, 90, 405-412.
3. Kelley, D. S., Siegel, D., Fedor, D. M., Adkins, Y. et al., DHA supplementation decreases serum C-reactive protein and other markers of inflammation in hypertriglyceridemic men. J. Nutr. 2009, 139, 495-501.
4. Cesari, M., Penninx, B. W., Newman, A. B., Kritchevsky, S. B. et al., Inflammatory markers and onset of cardiovascular events: results from the Health ABC study. Circulation 2003, 108, 2317-2322.
5. Itariu, B. K., Zeyda, M., Hochbrugger, E. E., Neuhofer, A. et al., Long-chain n-3 PUFAs reduce adipose tissue and systemic inflammation in severely obese nondiabetic patients: a randomized controlled trial. Am. J. Clin. Nutr. 2012, 96, 1137-1149.
6. Tekpli, X., Landvik, N. E., Anmarkud, K. H., Skaug, V. et al., DNA methylation at promoter regions of interleukin 1B, interleukin 6, and interleukin 8 in non-small cell lung cancer. Cancer Immunol. Immunother. 2013, 62, 337-345.
7. Stefani, F. A., Viana, M. B., Dupim, A. C., Brito, J. A. et al., Expression, polymorphism and methylation pattern of interleukin-6 in periodontal tissues. Immunobiology 2013, 218, 1012-1017.
8. Nile, C. J., Read, R. C., Akil, M., Duff, G. W. et al., Methylation status of a single CpG site in the IL6 promoter is related to IL6 messenger RNA levels and rheumatoid arthritis. Arthritis Rheum. 2008, 58, 2686-2693.
9. Dandrea, M., Donadelli, M., Costanzo, C., Scarpa, A. et al., MeCP2/H3meK9 are involved in IL-6 gene silencing in pancreatic adenocarcinoma cell lines. Nucleic Acids Res. 2009, 37, 6681-6690.
10. Zhi, D., Aslibekyan, S., Irvin, M. R., Claas, S. A. et al., SNPs located at CpG sites modulate genome-epigenome interaction. Epigenetics 2013, 8, 802-806.
11. Kanoni, S., Dedoussis, G. V., Herbein, G., Fulop, T. et al., Assessment of gene-nutrient interactions on inflammatory status of the elderly with the use of a zinc diet score-ZINCAGE study. J. Nutr. Biochem 2010, 21, 526-531.
12. Shin, K. K., Jang, Y., Koh, S. J., Chae, J. S. et al., Influence of the IL-6 -572C>G polymorphism on inflammatory markers according to cigarette smoking in Korean healthy men. Cytokine 2007, 39, 116-122.
13. Sunyer, J., Forastiere, F., Pekkanen, J., Plana, E. et al., Interaction between smoking and the interleukin-6 gene affects systemic levels of inflammatory biomarkers. Nicotine Tob. Res. 2009, 11, 1347-1353.
14. Sanderson, S. C., Kumari, M., Brunner, E. J., Miller, M. A. et al., Association between IL6 gene variants -174G>C and -572G>C and serum IL-6 levels: interactions with social position in the Whitehall II cohort. Atherosclerosis 2009, 204, 459-464.
15. Higgins, M., Province, M., Heiss, G., Eckfeldt, J. et al., NHLBI Family Heart Study: objectives and design. Am. J. Epidemiol. 1996, 143, 1219-1228.
16. Corella, D., Arnett, D. K., Tsai, M. Y., Kabagambe, E. K. et al., The -256T>C polymorphism in the apolipoprotein A-II gene promoter is associated with body mass index and food intake in the genetics of lipid lowering drugs and diet network study. Clin. Chem. 2007, 53, 1144-1152.
17. Georgiadou, P., Sbarouni, E., Effect of hormone replacement therapy on inflammatory biomarkers. Adv. Clin. Chem. 2009, 47, 59-93.
18. Tsai, M. Y., Hanson, N. Q., Straka, R. J., Hoke, T. R. et al., Effect of influenza vaccine on markers of inflammation and lipid profile. J. Lab. Clin. Med. 2005, 145, 323-327.
19. Aslibekyan, S., Kabagambe, E. K., Irvin, M. R., Straka, R. J. et al., A genome-wide association study of inflammatory biomarker changes in response to fenofibrate treatment in the Genetics of Lipid Lowering Drug and Diet Network. Pharmacogenet. Genomics 2012, 22, 191-197.
20. Shen, J., Arnett, D. K., Peacock, J. M., Parnell, L. D. et al., Interleukin1beta genetic polymorphisms interact with polyunsaturated fatty acids to modulate risk of the metabolic syndrome. J. Nutr. 2007, 137, 1846-1851.
21. Cao, J., Schwichtenberg, K. A., Hanson, N. Q., Tsai, M. Y., Incorporation and clearance of omega-3 fatty acids in erythrocyte membranes and plasma phospholipids. Clin. Chem. 2006, 52, 2265-2272.
22. Kabagambe, E. K., Ordovas, J. M., Tsai, M. Y., Borecki, I. B. et al., Smoking, inflammatory patterns and postprandial hypertriglyceridemia. Atherosclerosis 2009, 203, 633-639.
23. Kabagambe, E. K., Tsai, M. Y., Hopkins, P. N., Ordovas, J. M. et al., Erythrocyte fatty acid composition and the metabolic syndrome: a National Heart, Lung, and Blood Institute GOLDN study. Clin. Chem. 2008, 54, 154-162.
24. Ma, Y., Smith, C. E., Lai, C. Q., Irvin, M. R. et al., Genetic variants modify the effect of age on APOE methylation in the Genetics of Lipid Lowering Drugs and Diet Network study. Aging Cell 2015, 14, 49-59.
25. Flanagan, J. M., Brook, M. N., Orr, N., Tomczyk, K. et al., Temporal stability and determinants of white blood cell DNA methylation in the breakthrough generations study. Cancer Epidemiol. Biomarkers Prev. 2015, 24, 221-229.
26. Frazier-Wood, A. C., Aslibekyan, S., Absher, D. M., Hopkins, P. H. et al., Methylation at CPT1A locus is associated with lipoprotein subfraction profiles. J. Lipid Res. 2014, 55, 1324-1330.
27. Brydon, L., Wright, C. E., O'Donnell, K., Zachary, I. et al., Stress-induced cytokine responses and central adiposity in young women. Int. J. Obes. 2008, 32, 443-450.
28. Duncan, B. B., Schmidt, M. I., Pankow, J. S., Ballantyne, C. M. et al., Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 2003, 52, 1799-1805.
29. Zhang, W., Wang, W., Yu, H., Zhang, Y. et al., Interleukin 6 underlies angiotensin II-induced hypertension and chronic renal damage. Hypertension 2012, 59, 136-144.
30. Schindler, R., Mancilla, J., Endres, S., Ghorbani, R. et al., Correlations and interactions in the production of interleukin-6 (IL-6), IL-1, and tumor necrosis factor (TNF) in human blood mononuclear cells: IL-6 suppresses IL-1 and TNF. Blood 1990, 75, 40-47.
31. Kim, C. S., Park, H. S., Kawada, T., Kim, J. H. et al., Circulating levels of MCP-1 and IL-8 are elevated in human obese subjects and associated with obesity-related parameters. Int. J. Obes. 2006, 30, 1347-1355.
32. Abke, S., Neumeier, M., Weigert, J., Wehrwein, G. et al., Adiponectin-induced secretion of interleukin-6 (IL-6), monocyte chemotactic protein-1 (MCP-1, CCL2) and interleukin-8 (IL-8, CXCL8) is impaired in monocytes from patients with type I diabetes. Cardiovasc. Diabetol. 2006, 5, 17.
33. Rishi, V., Bhattacharya, P., Chatterjee, R., Rozenberg, J. et al., CpG methylation of half-CRE sequences creates C/EBPalpha binding sites that activate some tissue-specific genes. Proc. Natl. Acad. Sci. U S A 2010, 107, 20311-20316.
34. Flower, K., Thomas, D., Heather, J., Ramasubramanyan, S. et al., Epigenetic control of viral life-cycle by a DNA-methylation dependent transcription factor. PLoS One 2011, 6, e25922.
35. Vinokurova, S., von Knebel Doeberitz, M., Differential methylation of the HPV 16 upstream regulatory region during epithelial differentiation and neoplastic transformation. PLoS One 2011, 6, e24451.
36. Weber, M., Hellmann, I., Stadler, M. B., Ramos, L. et al., Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 2007, 39, 457-466.
37. De Felice, C., Cortelazzo, A., Signorini, C., Guerranti, R. et al., Effects of omega-3 polyunsaturated fatty acids on plasma proteome in Rett syndrome. Mediators Inflamm. 2013, 2013, 723269.
38. De Felice, C., Signorini, C., Leoncini, S., Pecorelli, A. et al., The role of oxidative stress in Rett syndrome: an overview. Ann. N Y Acad. Sci. 2012, 1259, 121-135.
39. Kerkel, K., Spadola, A., Yuan, E., Kosek, J. et al., Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation. Nat. Genet. 2008, 40, 904-908.
40. Lienert, F., Wirbelauer, C., Som, I., Dean, A. et al., Identification of genetic elements that autonomously determine DNA methylation states. Nat. Genet. 2011, 43, 1091-1097.
41. Smith, C. E., Follis, J. L., Nettleton, J. A., Foy, M. et al., Dietary fatty acids modulate associations between genetic variants and circulating fatty acids in plasma and erythrocyte membranes: meta-analysis of nine studies in the CHARGE consortium. Mol. Nutr. Food Res. 2015, 59, 1373-1383.