Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2016, Article ID 8539057, 11 pages
http://dx.doi.org/10.1155/2016/8539057
Research Article

Altered Methylation Profile of Lymphocytes Is Concordant with Perturbation of Lipids Metabolism and Inflammatory Response in Obesity

1Animal Genetics, Department of Veterinary Clinical and Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg, Denmark
2Sorbonne Universités, UPMC Univ Paris 06, INSERM UMR_S 1166, Integrative Biology of Atherosclerosis Team, 75013 Paris, France
3Institute of Cardiometabolism and Nutrition (ICAN), Pitié-Salpêtrière Hospital, 75013 Paris, France
4The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200 Copenhagen, Denmark
5Inflammation and Infection Research, School of Medical Sciences, UNSW Australia, Sydney, NSW 2052, Australia

Received 9 June 2015; Revised 31 August 2015; Accepted 6 September 2015

Academic Editor: Ed Randell

Copyright © 2016 Mette J. Jacobsen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. D. Pedersen, “Metabolic complications of obesity,” Best Practice & Research: Clinical Endocrinology & Metabolism, vol. 27, no. 2, pp. 179–193, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. S. W. P. Koppe, “Obesity and the liver: nonalcoholic fatty liver disease,” Translational Research, vol. 164, no. 4, pp. 312–322, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. S. H. Davoodi, T. Malek-Shahabi, A. Malekshahi-Moghadam, R. Shahbazi, and S. Esmaeili, “Obesity as an important risk factor for certain types of cancer,” Iranian Journal of Cancer Prevention, vol. 6, no. 4, pp. 186–194, 2013. View at Google Scholar · View at Scopus
  4. S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante Jr., “Obesity is associated with macrophage accumulation in adipose tissue,” The Journal of Clinical Investigation, vol. 112, no. 12, pp. 1796–1808, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Aron-Wisnewsky, J. Tordjman, C. Poitou et al., “Human adipose tissue macrophages: M1 and M2 cell surface markers in subcutaneous and omental depots and after weight loss,” The Journal of Clinical Endocrinology & Metabolism, vol. 94, no. 11, pp. 4619–4623, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Y. Oh, H. Morinaga, S. Talukdar, E. J. Bae, and J. M. Olefsky, “Increased macrophage migration into adipose tissue in obese mice,” Diabetes, vol. 61, no. 2, pp. 346–354, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. J. DeFuria, A. C. Belkina, M. Jagannathan-Bogdan et al., “B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 13, pp. 5133–5138, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Nishimura, I. Manabe, M. Nagasaki et al., “CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity,” Nature Medicine, vol. 15, no. 8, pp. 914–920, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. M. F. Gregor and G. S. Hotamisligil, “Inflammatory mechanisms in obesity,” Annual Review of Immunology, vol. 29, pp. 415–445, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Sell and J. Eckel, “Chemotactic cytokines, obesity and type 2 diabetes: in vivo and in vitro evidence for a possible causal correlation?” Proceedings of the Nutrition Society, vol. 68, no. 4, pp. 378–384, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. V. D. F. de Mello, L. Pulkkinen, M. Lalli, M. Kolehmainen, J. Pihlajamäki, and M. Uusitupa, “DNA methylation in obesity and type 2 diabetes,” Annals of Medicine, vol. 46, no. 3, pp. 103–113, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. S. J. van Dijk, P. L. Molloy, H. Varinli et al., “Epigenetics and human obesity,” International Journal of Obesity, vol. 39, no. 1, pp. 85–97, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. X. Wang, H. Zhu, H. Snieder et al., “Obesity related methylation changes in DNA of peripheral blood leukocytes,” BMC Medicine, vol. 8, article 87, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Simar, S. Versteyhe, I. Donkin et al., “DNA methylation is altered in B and NK lymphocytes in obese and type 2 diabetic human,” Metabolism: Clinical and Experimental, vol. 63, no. 9, pp. 1188–1197, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. X. Xu, S. Su, V. A. Barnes et al., “A genome-wide methylation study on obesity: differential variability and differential methylation,” Epigenetics, vol. 8, no. 5, pp. 522–533, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. P. C. J. Janson, L. B. Linton, E. A. Bergman et al., “Profiling of CD4+ T cells with epigenetic immune lineage analysis,” Journal of Immunology, vol. 186, no. 1, pp. 92–102, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Yang, X. Wang, D. Liu, L. Yu, B. Xue, and H. Shi, “Epigenetic regulation of macrophage polarization by DNA methyltransferase 3b,” Molecular Endocrinology, vol. 28, no. 4, pp. 565–574, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Maier, R. Ostraat, H. Gao et al., “Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription,” Nature Immunology, vol. 5, no. 10, pp. 1069–1077, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. H. H. Hermsdorff, M. L. Mansego, J. Campión, F. I. Milagro, M. A. Zulet, and J. A. Martínez, “TNF-alpha promoter methylation in peripheral white blood cells: relationship with circulating TNFalpha, truncal fat and n-6 PUFA intake in young women,” Cytokine, vol. 64, no. 1, pp. 265–271, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. M. C. García-Cardona, F. Huang, J. M. García-Vivas et al., “DNA methylation of leptin and adiponectin promoters in children is reduced by the combined presence of obesity and insulin resistance,” International Journal of Obesity, vol. 38, no. 11, pp. 1457–1465, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. M. E. Spurlock and N. K. Gabler, “The development of porcine models of obesity and the metabolic syndrome,” The Journal of Nutrition, vol. 138, no. 2, pp. 397–402, 2008. View at Google Scholar · View at Scopus
  22. M. A. Groenen, A. L. Archibald, H. Uenishi et al., “Analyses of pig genomes provide insight into porcine demography and evolution,” Nature, vol. 491, no. 7424, pp. 393–398, 2012. View at Publisher · View at Google Scholar
  23. H. D. Dawson, “Comparative assessment of the pig, mouse, and human genomes; a structural and functional analysis of genes involved in immunity,” in The Minipig in Biomedical Research P A McAnulty, A. Dayan and K. Hastings, Eds., p. 11, CRC Press, Taylor & Francis Group, 2011. View at Google Scholar
  24. L. J. A. Kogelman, H. N. Kadarmideen, T. Mark et al., “An F2 pig resource population as a model for genetic studies of obesity and obesity-related diseases in humans: design and genetic parameters,” Frontiers in Genetics, vol. 4, article 29, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Christoffersen, V. Golozoubova, G. Pacini, O. Svendsen, and K. Raun, “The young Göttingen minipig as a model of childhood and adolescent obesity: influence of diet and gender,” Obesity, vol. 21, no. 1, pp. 149–158, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. W. T. Friedewald, R. I. Levy, and D. S. Fredrickson, “Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge,” Clinical Chemistry, vol. 18, no. 6, pp. 499–502, 1972. View at Google Scholar · View at Scopus
  27. P. Decaunes, D. Estève, A. Zakaroff-Girard, C. Sengenès, J. Galitzky, and A. Bouloumié, “Adipose-derived stromal cells: cytokine expression and immune cell contaminants,” Methods in Molecular Biology, vol. 702, pp. 151–161, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Cirera, “Highly efficient method for isolation of total RNA from adipose tissue,” BMC Research Notes, vol. 6, article 472, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Traini, C. M. Quinn, C. Sandoval et al., “Sphingomyelin phosphodiesterase acid-like 3A (SMPDL3A) is a novel nucleotide phosphodiesterase regulated by cholesterol in human macrophages,” The Journal of Biological Chemistry, vol. 289, no. 47, pp. 32895–32913, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. T. M. Foy, A. Aruffo, J. Bajorath, J. E. Buhlmann, and R. J. Noelle, “Immune regulation by CD40 and its ligand GP39,” Annual Review of Immunology, vol. 14, pp. 591–617, 1996. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Wueest, R. Mueller, M. Blüher et al., “Fas (CD95) expression in myeloid cells promotes obesity-induced muscle insulin resistance,” EMBO Molecular Medicine, vol. 6, no. 1, pp. 43–56, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. Y.-T. Huang, J. Z. J. Maccani, N. L. Hawley, R. R. Wing, K. T. Kelsey, and J. M. McCaffery, “Epigenetic patterns in successful weight loss maintainers: a pilot study,” International Journal of Obesity, vol. 39, no. 5, pp. 865–868, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. A. E. Newell-Fugate, J. N. Taibl, S. G. Clark, M. Alloosh, M. Sturek, and R. L. Krisher, “Effects of diet-induced obesity on metabolic parameters and reproductive function in female ossabaw minipigs,” Comparative Medicine, vol. 64, no. 1, pp. 44–49, 2014. View at Google Scholar · View at Scopus
  34. S. Cirera, M. S. Jensen, V. S. Elbrønd et al., “Expression studies of six human obesity-related genes in seven tissues from divergent pig breeds,” Animal Genetics, vol. 45, no. 1, pp. 59–66, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. R. J. Faris, R. L. Boddicker, J. Walker-Daniels, J. Li, D. E. Jones, and M. E. Spurlock, “Inflammation in response to n3 fatty acids in a porcine obesity model,” Comparative Medicine, vol. 62, no. 6, pp. 495–503, 2012. View at Google Scholar · View at Scopus
  36. A. S. Pawar, X.-Y. Zhu, A. Eirin et al., “Adipose tissue remodeling in a novel domestic porcine model of diet-induced obesity,” Obesity, vol. 23, no. 2, pp. 399–407, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. S. U. Amano, J. L. Cohen, P. Vangala et al., “Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation,” Cell Metabolism, vol. 19, no. 1, pp. 162–171, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. P. S. Patel, E. D. Buras, and A. Balasubramanyam, “The role of the immune system in obesity and insulin resistance,” Journal of Obesity, vol. 2013, Article ID 616193, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. U. Kintscher, M. Hartge, K. Hess et al., “T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 7, pp. 1304–1310, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Deiuliis, Z. Shah, N. Shah et al., “Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers,” PLoS ONE, vol. 6, no. 1, Article ID e16376, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Winer, Y. Chan, G. Paltser et al., “Normalization of obesity-associated insulin resistance through immunotherapy,” Nature Medicine, vol. 15, no. 8, pp. 921–929, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Cipolletta, M. Feuerer, A. Li et al., “PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue T reg cells,” Nature, vol. 486, no. 7404, pp. 549–553, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Yao, O. Herlea-Pana, J. Heuser-Baker, Y. Chen, and J. Barlic-Dicen, “Roles of the chemokine system in development of obesity, insulin resistance, and cardiovascular disease,” Journal of Immunology Research, vol. 2014, Article ID 181450, 11 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Carbone, C. La Rocca, and G. Matarese, “Immunological functions of leptin and adiponectin,” Biochimie, vol. 94, no. 10, pp. 2082–2088, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. S. A. Lund, C. M. Giachelli, and M. Scatena, “The role of osteopontin in inflammatory processes,” Journal of Cell Communication and Signaling, vol. 3, no. 3-4, pp. 311–322, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Ingvorsen, A. H. Thysen, D. Fernandez-Twinn et al., “Effects of pregnancy on obesity-induced inflammation in a mouse model of fetal programming,” International Journal of Obesity, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Wolf, F. Jehle, N. A. Michel et al., “Coinhibitory suppression of T cell activation by CD40 protects against obesity and adipose tissue inflammation in mice,” Circulation, vol. 129, no. 23, pp. 2414–2425, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Dhein, H. Walczak, C. Baumler, K.-M. Debatin, and P. H. Krammer, “Autocrine T-cell suicide mediated by APO-1/(Fas/CD95),” Nature, vol. 373, no. 6513, pp. 438–441, 1995. View at Publisher · View at Google Scholar · View at Scopus
  49. L. Catrysse, L. Vereecke, R. Beyaert, and G. van Loo, “A20 in inflammation and autoimmunity,” Trends in Immunology, vol. 35, no. 1, pp. 22–31, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Matmati, P. Jacques, J. Maelfait et al., “A20 (TNFAIP3) deficiency in myeloid cells triggers erosive polyarthritis resembling rheumatoid arthritis,” Nature Genetics, vol. 43, no. 9, pp. 908–912, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. C.-H. Tsao, M.-Y. Shiau, P.-H. Chuang, Y.-H. Chang, and J. Hwang, “Interleukin-4 regulates lipid metabolism by inhibiting adipogenesis and promoting lipolysis,” Journal of Lipid Research, vol. 55, no. 3, pp. 385–397, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. B. R. Lawson, T. Eleftheriadis, V. Tardif et al., “Transmethylation in immunity and autoimmunity,” Clinical Immunology, vol. 143, no. 1, pp. 8–21, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. D. A. Winer, S. Winer, L. Shen et al., “B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies,” Nature Medicine, vol. 17, no. 5, pp. 610–617, 2011. View at Publisher · View at Google Scholar · View at Scopus