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Mediators of Inflammation
Volume 2013 (2013), Article ID 808125, 14 pages
http://dx.doi.org/10.1155/2013/808125
Review Article

Rheumatic Diseases and Obesity: Adipocytokines as Potential Comorbidity Biomarkers for Cardiovascular Diseases

1Dipartimento di Medicina Interna e Specialità Mediche, Reumatologia, Sapienza Università di Roma, Viale del Policlinico 155, 00161 Rome, Italy
2Department of Rheumatology and Immunology, University of Gießen, Kerckhoff Klinik, Benekestr 2-8, 61231 Bad Nauheim, Germany

Received 15 May 2013; Revised 29 October 2013; Accepted 30 October 2013

Academic Editor: Eric F. Morand

Copyright © 2013 Rossana Scrivo 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. 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,” Journal of Clinical Investigation, vol. 112, no. 12, pp. 1796–1808, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Tilg and A. R. Moschen, “Adipocytokines: mediators linking adipose tissue, inflammation and immunity,” Nature Reviews Immunology, vol. 6, no. 10, pp. 772–783, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. S. S. Martin, A. Qasim, and M. P. Reilly, “Leptin resistance. A possible interface of inflammation and metabolism in obesity-related cardiovascular disease,” Journal of the American College of Cardiology, vol. 52, no. 15, pp. 1201–1210, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Luk, Z. Malam, and J. C. Marshall, “Pre-B cell colony-enhancing factor (PBEF)/visfatin: a novel mediator of innate immunity,” Journal of Leukocyte Biology, vol. 83, no. 4, pp. 804–816, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Blüher, “Do adipokines link obesity to its related metabolic and cardiovascular diseases?” Clinical Lipidology, vol. 5, no. 1, pp. 95–107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. H. E. Bays, “‘Sick fat,’ metabolic disease, and atherosclerosis,” The American Journal of Medicine, vol. 122, supplement 1, pp. S26–S37, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Jenkins, A. Flynn, T. Smart et al., “A statistician's perspective on biomarkers in drug development,” Pharmaceutical Statistics, vol. 10, no. 6, pp. 494–507, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. C. S. Crowson, E. L. Matteson, J. M. Davis III, and S. E. Gabriel, “Contribution of obesity to the rise in incidence of rheumatoid arthritis,” Arthritis Care and Research, vol. 65, no. 1, pp. 71–77, 2013. View at Publisher · View at Google Scholar
  9. Ajeganova, M. L. Andersson, I. Hafström, and BARFOT Study Group, “Obesity is associated with worse disease severity in rheumatoid arthritis as well as with co-morbidities—a long-term follow-up from disease onset,” Arthritis Care and Research, vol. 65, no. 1, pp. 78–87, 2013. View at Publisher · View at Google Scholar
  10. L. S. Lohmander, M. G. de Verdier, J. Rollof, P. M. Nilsson, and G. Engström, “Incidence of severe knee and hip osteoarthritis in relation to different measures of body mass: a population-based prospective cohort study,” Annals of the Rheumatic Diseases, vol. 68, no. 4, pp. 490–496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. World Health Organization, Health Topics: Obesity, World Health Organization, Geneva, Switzerland, 2011, http://www.who.int/topics/obesity/en/.
  12. L. F. van Gaal, I. L. Mertens, and C. E. de Block, “Mechanisms linking obesity with cardiovascular disease,” Nature, vol. 444, no. 7121, pp. 875–880, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Leroith, R. Novosyadlyy, E. J. Gallagher, D. Lann, A. Vljayakumar, and S. Yakar, “Obesity and Type 2 diabetes are associated with an increased risk of developing cancer and a worse prognosis; epidemiological and mechanistic evidence,” Experimental and Clinical Endocrinology and Diabetes, vol. 116, supplement 1, pp. S4–S6, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Blüher, “Adipose tissue dysfunction in obesity,” Experimental and Clinical Endocrinology and Diabetes, vol. 117, no. 6, pp. 241–250, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Sarraf, R. C. Frederich, E. M. Turner et al., “Multiple cytokines and acute inflammation raise mouse leptin levels: potential role in inflammatory anorexia,” Journal of Experimental Medicine, vol. 185, no. 1, pp. 171–175, 1997. View at Publisher · View at Google Scholar · View at Scopus
  16. R. S. Ahima, D. Prabakaran, C. Mantzoros et al., “Role of leptin in the neuroendocrine response to fasting,” Nature, vol. 382, no. 6588, pp. 250–252, 1996. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Hotta, T. Funahashi, N. L. Bodkin et al., “Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys,” Diabetes, vol. 50, no. 5, pp. 1126–1133, 2001. View at Google Scholar · View at Scopus
  18. N. Maeda, I. Shimomura, K. Kishida et al., “Diet-induced insulin resistance in mice lacking adiponectin/ACRP30,” Nature Medicine, vol. 8, no. 7, pp. 731–737, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Patel, A. C. Buckels, I. J. Kinghorn et al., “Resistin is expressed in human macrophages and directly regulated by PPARγ activators,” Biochemical and Biophysical Research Communications, vol. 300, no. 2, pp. 472–476, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. C. A. Curat, V. Wegner, C. Sengenès et al., “Macrophages in human visceral adipose tissue: increased accumulation in obesity and a source of resistin and visfatin,” Diabetologia, vol. 49, no. 4, pp. 744–747, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Stastny, J. Bienertova-Vasku, and A. Vasku, “Visfatin and its role in obesity development,” Diabetes and Metabolic Syndrome, vol. 6, no. 2, pp. 120–124, 2012. View at Publisher · View at Google Scholar
  22. M. P. Chen, F. M. Chung, D. M. Chang et al., “Elevated plasma level of visfatin/pre-B cell colony-enhancing factor in patients with type 2 diabetes mellitus,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 1, pp. 295–299, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. C. M. Steppan, S. T. Bailey, S. Bhat et al., “The hormone resistin links obesity to diabetes,” Nature, vol. 409, no. 6818, pp. 307–312, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. S. M. Rangwala, A. S. Rich, B. Rhoades et al., “Abnormal glucose homeostasis due to chronic hyperresistinemia,” Diabetes, vol. 53, no. 8, pp. 1937–1941, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. J. M. Friedman, “Leptin and the regulation of body weight,” Keio Journal of Medicine, vol. 60, no. 1, pp. 1–9, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Boden, X. Chen, M. Mozzoli, and I. Ryan, “Effect of fasting on serum leptin in normal human subjects,” Journal of Clinical Endocrinology and Metabolism, vol. 81, no. 9, pp. 3419–3423, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. J. W. Kolaczynski, J. P. Ohannesian, R. V. Considine, C. C. Marco, and J. F. Caro, “Response of leptin to short-term and prolonged overfeeding in humans,” Journal of Clinical Endocrinology and Metabolism, vol. 81, no. 11, pp. 4162–4165, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Boden, X. Chen, J. W. Kolaczynski, and M. Polansky, “Effects of prolonged hyperinsulinemia on serum leptin in normal human subjects,” Journal of Clinical Investigation, vol. 100, no. 5, pp. 1107–1113, 1997. View at Google Scholar · View at Scopus
  29. R. S. Ahima and J. S. Flier, “Leptin,” Annual Review of Physiology, vol. 62, pp. 413–437, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. N. Maeda, M. Takahashi, T. Funahashi et al., “PPARγ ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein,” Diabetes, vol. 50, no. 9, pp. 2094–2099, 2001. View at Google Scholar · View at Scopus
  31. Y. Arita, S. Kihara, N. Ouchi et al., “Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity,” Biochemical and Biophysical Research Communications, vol. 257, no. 1, pp. 79–83, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. K. W. Frommer, A. Schäffler, C. Büchler et al., “Adiponectin isoforms: a potential therapeutic target in rheumatoid arthritis?” Annals of the Rheumatic Diseases, vol. 71, no. 10, pp. 1724–1732, 2012. View at Publisher · View at Google Scholar
  33. R. Baratta, S. Amato, C. Degano et al., “Adiponectin relationship with lipid metabolism is independent of body fat mass: evidence from both cross-sectional and intervention studies,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 6, pp. 2665–2671, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Hung, B. M. McQuillan, P. L. Thompson, and J. P. Beilby, “Circulating adiponectin levels associate with inflammatory markers, insulin resistance and metabolic syndrome independent of obesity,” International Journal of Obesity, vol. 32, no. 5, pp. 772–779, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. J. M. Dekker, T. Funahashi, G. Nijpels et al., “Prognostic value of adiponectin for cardiovascular disease and mortality,” Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 4, pp. 1489–1496, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Li, H. J. Shin, E. L. Ding, and R. M. van Dam, “Adiponectin levels and risk of type 2 diabetes: a systematic review and meta-analysis,” The Journal of the American Medical Association, vol. 302, no. 2, pp. 179–188, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Tucholski and E. Otto-Buczkowska, “The role of leptin in the regulation of carbohydrate metabolism,” Polish Journal of Endocrinology, vol. 62, no. 3, pp. 258–262, 2011. View at Google Scholar · View at Scopus
  38. Y. Tabara, H. Osawa, R. Kawamoto et al., “Reduced high-molecular-weight adiponectin and elevated high-sensitivity C-reactive protein are synergistic risk factors for metabolic syndrome in a large-scale middle-aged to elderly population: the Shimanami health promoting program study,” Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 3, pp. 715–722, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Rizza, F. Gigli, A. Galli et al., “Adiponectin isoforms in elderly patients with or without coronary artery disease,” Journal of the American Geriatrics Society, vol. 58, no. 4, pp. 702–706, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Nakashima, K. Yamane, N. Kamei, S. Nakanishi, and N. Kohno, “Low serum levels of total and high-molecular-weight adiponectin predict the development of metabolic syndrome in Japanese-Americans,” Journal of Endocrinological Investigation, vol. 34, no. 8, pp. 615–619, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Graessler, M. Gruber, R. Radke et al., “Type 2 diabetes in octogenarians is associated with decreased low molecular weight adiponectin,” Gerontology, vol. 57, no. 4, pp. 316–326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. R. Moschen, A. Kaser, B. Enrich et al., “Visfatin, an adipocytokine with proinflammatory and immunomodulating properties,” Journal of Immunology, vol. 178, no. 3, pp. 1748–1758, 2007. View at Google Scholar · View at Scopus
  43. P. Wang, M. M. J. van Greevenbroek, F. G. Bouwman et al., “The circulating PBEF/NAMPT/visfatin level is associated with a beneficial blood lipid profile,” Pflügers Archiv, vol. 454, no. 6, pp. 971–976, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Sentinelli, S. Romeo, M. Arca et al., “Human resistin gene, obesity, and type 2 diabetes: mutation analysis and population study,” Diabetes, vol. 51, no. 3, pp. 860–862, 2002. View at Google Scholar · View at Scopus
  45. M. Degawa-Yamauchi, J. E. Bovenkerk, B. E. Juliar et al., “Serum resistin (FIZZ3) protein is increased in obese humans,” Journal of Clinical Endocrinology and Metabolism, vol. 88, no. 11, pp. 5452–5455, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. J. H. Lee, J. L. Chan, N. Yiannakouris et al., “Circulating resistin levels are not associated with obesity or insulin resistance in humans and are not regulated by fasting or leptin administration: cross-sectional and interventional studies in normal, insulin-resistant, and diabetic subjects,” Journal of Clinical Endocrinology and Metabolism, vol. 88, no. 10, pp. 4848–4856, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. L. K. Heilbronn, J. Rood, L. Janderova et al., “Relationship between serum resistin concentrations and insulin resistance in nonobese, obese, and obese diabetic subjects,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 4, pp. 1844–1848, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Vozarova de Courten, M. Degawa-Yamauchi, R. V. Considine, and P. A. Tataranni, “High serum resistin is associated with an increase in adiposity but not a worsening of insulin resistance in Pima Indians,” Diabetes, vol. 53, no. 5, pp. 1279–1284, 2004. View at Google Scholar
  49. M. P. Reilly, M. Lehrke, M. L. Wolfe, A. Rohatgi, M. A. Lazar, and D. J. Rader, “Resistin is an inflammatory marker of atherosclerosis in humans,” Circulation, vol. 111, no. 7, pp. 932–939, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. M. F. Hivert, L. M. Sullivan, C. S. Fox et al., “Associations of adiponectin, resistin, and tumor necrosis factor-α with insulin resistance,” Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 8, pp. 3165–3172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Beckers, D. Zegers, J. K. van Camp et al., “Resistin polymorphisms show associations with obesity, but not with bone parameters in men: results from the odense androgen study,” Molecular Biology Reports, vol. 40, no. 3, pp. 2467–2472, 2013. View at Publisher · View at Google Scholar
  52. E. J. B. Ramos, Y. Xu, I. Romanova et al., “Is obesity an inflammatory disease?” Surgery, vol. 134, no. 2, pp. 329–335, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. G. S. Hotamisligil, N. S. Shargill, and B. M. Spiegelman, “Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance,” Science, vol. 259, no. 5091, pp. 87–91, 1993. View at Google Scholar · View at Scopus
  54. J. A. Aviña-Zubieta, H. K. Choi, M. Sadatsafavi, M. Etminan, J. M. Esdaile, and D. Lacaille, “Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies,” Arthritis Care and Research, vol. 59, no. 12, pp. 1690–1697, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Otero, R. Logo, R. Gomez et al., “Changes in plasma levels of fat-derived hormones adiponectin, leptin, resistin and visfatin in patients with rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 65, no. 9, pp. 1198–1201, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. S. W. Lee, M. C. Park, Y. B. Park, and S. K. Lee, “Measurement of the serum leptin level could assist disease activity monitoring in rheumatoid arthritis,” Rheumatology International, vol. 27, no. 6, pp. 537–540, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Schäffler, A. Ehling, E. Neumann et al., “Adipocytokines in synovial fluid,” The Journal of the American Medical Association, vol. 290, no. 13, pp. 1709–1710, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Kenchaiah, J. C. Evans, D. Levy et al., “Obesity and the risk of heart failure,” The New England Journal of Medicine, vol. 347, no. 5, pp. 305–313, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Yoda-Murakami, M. Taniguchi, K. Takahashi et al., “Change in expression of GBP28/adiponectin in carbon tetrachloride-administrated mouse liver,” Biochemical and Biophysical Research Communications, vol. 285, no. 2, pp. 372–377, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. H. S. Berner, S. P. Lyngstadaas, A. Spahr et al., “Adiponectin and its receptors are expressed in bone-forming cells,” Bone, vol. 35, no. 4, pp. 842–849, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. A. M. Delaigle, J. Jonas, I. B. Bauche, O. Cornu, and S. M. Brichard, “Induction of adiponectin in skeletal muscle by inflammatory cytokines: in vivo and in vitro studies,” Endocrinology, vol. 145, no. 12, pp. 5589–5597, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Ehling, A. Schäffler, H. Herfarth et al., “The potential of adiponectin in driving arthritis,” Journal of Immunology, vol. 176, no. 7, pp. 4468–4478, 2006. View at Google Scholar
  63. N. Ouchi, S. Kihara, Y. Arita et al., “Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin,” Circulation, vol. 100, no. 25, pp. 2473–2476, 1999. View at Google Scholar · View at Scopus
  64. K. W. Frommer, B. Zimmermann, F. M. P. Meier et al., “Adiponectin-mediated changes in effector cells involved in the pathophysiology of rheumatoid arthritis,” Arthritis and Rheumatism, vol. 62, no. 10, pp. 2886–2899, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. H. M. Choi, Y. A. Lee, S. H. Lee et al., “Adiponectin may contribute to synovitis and joint destruction in rheumatoid arthritis by stimulating vascular endothelial growth factor, matrix metalloproteinase-1, and matrix metalloproteinase-13 expression in fibroblast-like synoviocytes more than proinflammatory mediators,” Arthritis Research and Therapy, vol. 11, no. 6, article R161, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. C. P. Chung, A. Oeser, J. F. Solus et al., “Inflammation-associated insulin resistance: differential effects in rheumatoid arthritis and systemic lupus erythematosus define potential mechanisms,” Arthritis and Rheumatism, vol. 58, no. 7, pp. 2105–2112, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. N. Busso, A. So, V. Chobaz-Péclat et al., “Leptin signaling deficiency impairs humoral and cellular immune responses and attenuates experimental arthritis,” Journal of Immunology, vol. 168, no. 2, pp. 875–882, 2002. View at Google Scholar · View at Scopus
  68. G. M. Lord, G. Matarese, J. K. Howard, R. J. Baker, S. R. Bloom, and R. I. Lechler, “Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression,” Nature, vol. 394, no. 6696, pp. 897–901, 1998. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Bokarewa, I. Nagaev, L. Dahlberg, U. Smith, and A. Tarkowski, “Resistin, an adipokine with potent proinflammatory properties,” Journal of Immunology, vol. 174, no. 9, pp. 5789–5795, 2005. View at Google Scholar · View at Scopus
  70. F. M. Meier, K. W. Frommer, M. A. Peters et al., “Visfatin/pre-B cell colony-enhancing factor (PBEF): a proinflammatory and cell motility-changing factor in rheumatoid arthritis,” The Journal of Biological Chemistry, vol. 287, no. 34, pp. 28378–28385, 2012. View at Publisher · View at Google Scholar
  71. A. Escalante, R. W. Haas, and I. del Rincón, “Paradoxical effect of body mass index on survival in rheumatoid arthritis: role of comorbidity and systemic inflammation,” Archives of Internal Medicine, vol. 165, no. 14, pp. 1624–1629, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. A. C. Elkan, I. L. Engvall, T. Cederholm, and I. Hafström, “Rheumatoid cachexia, central obesity and malnutrition in patients with low-active rheumatoid arthritis: feasibility of anthropometry, mini nutritional assessment and body composition techniques,” European Journal of Nutrition, vol. 48, no. 5, pp. 315–322, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. P. H. Dessein and B. I. Joffe, “Insulin resistance and impaired beta cell function in rheumatoid arthritis,” Arthritis and Rheumatism, vol. 54, no. 9, pp. 2765–2775, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. T. A. Pearson, G. A. Mensah, R. W. Alexander et al., “Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the centers for disease control and prevention and the American heart association,” Circulation, vol. 107, no. 3, pp. 499–511, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Tomizawa, Y. Hattori, K. Kasai, and Y. Nakano, “Adiponectin induces NF-κB activation that leads to suppression of cytokine-induced NF-κB activation in vascular endothelial cells: globular adiponectin versus high molecular weight adiponectin,” Diabetes and Vascular Disease Research, vol. 5, no. 2, pp. 123–127, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. Y. Hattori, Y. Nakano, S. Hattori, A. Tomizawa, K. Inukai, and K. Kasai, “High molecular weight adiponectin activates AMPK and suppresses cytokine-induced NF-κB activation in vascular endothelial cells,” FEBS Letters, vol. 582, no. 12, pp. 1719–1724, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. K. Ebina, A. Fukuhara, W. Ando et al., “Serum adiponectin concentrations correlate with severity of rheumatoid arthritis evaluated by extent of joint destruction,” Clinical Rheumatology, vol. 28, no. 4, pp. 445–451, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. J. T. Giles, D. M. van der Heijde, and J. M. Bathon, “Association of circulating adiponectin levels with progression of radiographic joint destruction in rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 70, no. 9, pp. 1562–1568, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. I. R. Klein-Wieringa, M. P. M. van der Linden, R. Knevel et al., “Baseline serum adipokine levels predict radiographic progression in early rheumatoid arthritis,” Arthritis and Rheumatism, vol. 63, no. 9, pp. 2567–2574, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. X. H. Luo, L. J. Guo, H. Xie et al., “Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway,” Journal of Bone and Mineral Research, vol. 21, no. 10, pp. 1648–1656, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. T. Alonzi, E. Fattori, D. Lazzaro et al., “Interleukin 6 is required for the development of collagen-induced arthritis,” Journal of Experimental Medicine, vol. 187, no. 4, pp. 461–468, 1998. View at Publisher · View at Google Scholar · View at Scopus
  82. C. Gabay, “Interleukin-6 and chronic inflammation,” Arthritis Research and Therapy, vol. 8, supplement 2, article S3, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. P. Härle, P. Sarzi-Puttini, M. Cutolo, and R. H. Straub, “No change of serum levels of leptin and adiponectin during anti-tumour necrosis factor antibody treatment with adalimumab in patients with rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 65, no. 7, pp. 970–971, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. T. B. Laurberg, J. Frystyk, T. Ellingsen et al., “Plasma adiponectin in patients with active, early, and chronic rheumatoid arthritis who are steroid- and disease-modifying antirheumatic drug-naive compared with patients with osteoarthritis and controls,” Journal of Rheumatology, vol. 36, no. 9, pp. 1885–1891, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. J. T. Giles, M. Allison, C. O. Bingham III, W. M. Scott Jr., and J. M. Bathon, “Adiponectin is a mediator of the inverse association of adiposity with radiographic damage in rheumatoid arthritis,” Arthritis Care and Research, vol. 61, no. 9, pp. 1248–1256, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. A. H. M. van der Helm-van Mil, S. M. van der Kooij, C. F. Allaart, R. E. M. Toes, and T. W. J. Huizinga, “A high body mass index has a protective effect on the amount of joint destruction in small joints in early rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 67, no. 6, pp. 769–774, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. H. P. Kopp, K. Krzyzanowska, M. Möhlig, J. Spranger, A. F. H. Pfeiffer, and G. Schernthaner, “Effects of marked weight loss on plasma levels of adiponectin, markers of chronic subclinical inflammation and insulin resistance in morbidly obese women,” International Journal of Obesity, vol. 29, no. 7, pp. 766–771, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. H. J. Anders, M. Rihl, A. Heufelder, O. Loch, and M. Schattenkirchner, “Leptin serum levels are not correlated with disease activity in patients with rheumatoid arthritis,” Metabolism, vol. 48, no. 6, pp. 745–748, 1999. View at Publisher · View at Google Scholar · View at Scopus
  89. C. Popa, M. G. Netea, T. R. D. S. Radstake, P. L. van Riel, P. Barrera, and J. W. M. van der Meer, “Markers of inflammation are negatively correlated with serum leptin in rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 64, no. 8, pp. 1195–1198, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. S. Hizmetli, M. Kisa, N. Gokalp, and M. Z. Bakici, “Are plasma and synovial fluid leptin levels correlated with disease activity in rheumatoid arthritis?” Rheumatology International, vol. 27, no. 4, pp. 335–338, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Wisłowska, M. Rok, B. Jaszczyk, K. Stȩpień, and M. Cicha, “Serum leptin in rheumatoid arthritis,” Rheumatology International, vol. 27, no. 10, pp. 947–954, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Salazar-Páramo, M. González-Ortiz, L. González-López et al., “Serum leptin levels in patients with rheumatoid arthritis,” Journal of Clinical Rheumatology, vol. 7, no. 1, pp. 57–59, 2001. View at Google Scholar
  93. M. Bokarewa, D. Bokarew, O. Hultgren, and A. Tarkowski, “Leptin consumption in the inflamed joints of patients with rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 62, no. 10, pp. 952–956, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. É. Toussirot, N. U. Nguyen, G. Dumoulin, F. Aubin, J. Cédoz, and D. Wendling, “Relationship between growth hormone-IGF-I-IGFBP-3 axis and serum leptin levels with bone mass and body composition in patients with rheumatoid arthritis,” Rheumatology, vol. 44, no. 1, pp. 120–125, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. Y. H. Rho, J. Solus, T. Sokka et al., “Adipocytokines are associated with radiographic joint damage in rheumatoid arthritis,” Arthritis and Rheumatism, vol. 60, no. 7, pp. 1906–1914, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. S. M. Olama, M. K. Senna, and M. Elarman, “Synovial/serum leptin ratio in rheumatoid arthritis: the association with activity and erosion,” Rheumatology International, vol. 32, no. 3, pp. 683–690, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. C. Gabay, M. G. Dreyer, N. Pellegrinelli, R. Chicheportiche, and C. A. Meier, “Leptin directly induces the secretion of interleukin 1 receptor antagonist in human monocytes,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 2, pp. 783–791, 2001. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Cohen, E. Hurd, J. Cush et al., “Treatment of rheumatoid arthritis with anakinra, a recombinant human interleukin-1 receptor antagonist, in combination with methotrexate: results of a twenty-four-week, multicenter, randomized, double-blind, placebo-controlled trial,” Arthritis and Rheumatism, vol. 46, no. 3, pp. 614–624, 2002. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. H. Rho, C. P. Chung, J. F. Solus et al., “Adipocytokines, insulin resistance, and coronary atherosclerosis in rheumatoid arthritis,” Arthritis and Rheumatism, vol. 62, no. 5, pp. 1259–1264, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. L. Šenolt, D. Housa, Z. Vernerová et al., “Resistin in rheumatoid arthritis synovial tissue, synovial fluid and serum,” Annals of the Rheumatic Diseases, vol. 66, no. 4, pp. 458–463, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. R. Klaasen, M. M. J. Herenius, C. A. Wijbrandts et al., “Treatment-specific changes in circulating adipocytokines: a comparison between tumour necrosis factor blockade and glucocorticoid treatment for rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 71, no. 9, pp. 1510–1516, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. J. W. J. Bijlsma, F. Berenbaum, and F. P. J. G. Lafeber, “Osteoarthritis: an update with relevance for clinical practice,” The Lancet, vol. 377, no. 9783, pp. 2115–2126, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. L. G. Alexopoulos, I. Youn, P. Bonaldo, and F. Guilak, “Developmental and osteoarthritic changes in Col6a1-knockout mice: biomechanics of type VI collagen in the cartilage pericellular matrix,” Arthritis and Rheumatism, vol. 60, no. 3, pp. 771–779, 2009. View at Publisher · View at Google Scholar · View at Scopus
  104. D. Iliopoulos, K. N. Malizos, and A. Tsezou, “Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention,” Annals of the Rheumatic Diseases, vol. 66, no. 12, pp. 1616–1621, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. E. Yusuf, R. G. Nelissen, A. Ioan-Facsinay et al., “Association between weight or body mass index and hand osteoarthritis: a systematic review,” Annals of the Rheumatic Diseases, vol. 69, no. 4, pp. 761–765, 2010. View at Publisher · View at Google Scholar · View at Scopus
  106. W. Hui, G. J. Litherland, M. S. Elias et al., “Leptin produced by joint white adipose tissue induces cartilage degradation via upregulation and activation of matrix metalloproteinases,” Annals of the Rheumatic Diseases, vol. 71, no. 3, pp. 455–462, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Liang, J. Feng, W. K. K. Wu et al., “Leptin-mediated cytoskeletal remodeling in chondrocytes occurs via the RhoA/ROCK pathway,” Journal of Orthopaedic Research, vol. 29, no. 3, pp. 369–374, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. T. M. Griffin, B. Fermor, J. L. Huebner et al., “Diet-induced obesity differentially regulates behavioral, biomechanical, and molecular risk factors for osteoarthritis in mice,” Arthritis Research and Therapy, vol. 12, no. 4, article R130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  109. T. Simopoulou, K. N. Malizos, D. Iliopoulos et al., “Differential expression of leptin and leptin's receptor isoform (Ob-Rb) mRNA between advanced and minimally affected osteoarthritic cartilage; effect on cartilage metabolism,” Osteoarthritis and Cartilage, vol. 15, no. 8, pp. 872–883, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. K. M. Tong, C. P. Chen, K. C. Huang et al., “Adiponectin increases MMP-3 expression in human chondrocytes through adipor1 signaling pathway,” Journal of Cellular Biochemistry, vol. 112, no. 5, pp. 1431–1440, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. E. H. Kang, Y. J. Lee, T. K. Kim et al., “Adiponectin is a potential catabolic mediator in osteoarthritis cartilage,” Arthritis Research and Therapy, vol. 12, no. 6, article R231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. R. Lago, R. Gomez, M. Otero et al., “A new player in cartilage homeostasis: adiponectin induces nitric oxide synthase type II and pro-inflammatory cytokines in chondrocytes,” Osteoarthritis and Cartilage, vol. 16, no. 9, pp. 1101–1109, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. T. H. Chen, L. Chen, M. S. Hsieh, C. P. Chang, D. T. Chou, and S. H. Tsai, “Evidence for a protective role for adiponectin in osteoarthritis,” Biochimica et Biophysica Acta, vol. 1762, no. 8, pp. 711–718, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. M. Gosset, F. Berenbaum, C. Salvat et al., “Crucial role of visfatin/pre-B cell colony-enhancing factor in matrix degradation and prostaglandin E2 synthesis in chondrocytes: possible influence on osteoarthritis,” Arthritis and Rheumatism, vol. 58, no. 5, pp. 1399–1409, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. R. R. Yammani and R. F. Loeser, “Extracellular nicotinamide phosphoribosyltransferase (NAMPT/visfatin) inhibits insulin-like growth factor-1 signaling and proteoglycan synthesis in human articular chondrocytes,” Arthritis Research and Therapy, vol. 14, no. 1, article R23, 2012. View at Publisher · View at Google Scholar · View at Scopus
  116. J. H. Lee, T. Ort, K. Ma et al., “Resistin is elevated following traumatic joint injury and causes matrix degradation and release of inflammatory cytokines from articular cartilage in vitro,” Osteoarthritis and Cartilage, vol. 17, no. 5, pp. 613–620, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. I. R. Klein-Wieringa, M. Kloppenburg, Y. M. Bastiaansen-Jenniskens et al., “The infrapatellar fat pad of patients with osteoarthritis has an inflammatory phenotype,” Annals of the Rheumatic Diseases, vol. 70, no. 5, pp. 851–857, 2011. View at Publisher · View at Google Scholar · View at Scopus
  118. S. Clockaerts, Y. M. Bastiaansen-Jenniskens, C. Feijt et al., “Cytokine production by infrapatellar fat pad can be stimulated by interleukin 1β and inhibited by peroxisome proliferator activated receptor α agonist,” Annals of the Rheumatic Diseases, vol. 71, no. 6, pp. 1012–1018, 2012. View at Publisher · View at Google Scholar · View at Scopus
  119. P. A. Berry, S. W. Jones, F. M. Cicuttini, A. E. Wluka, and R. A. MacIewicz, “Temporal relationship between serum adipokines, biomarkers of bone and cartilage turnover, and cartilage volume loss in a population with clinical knee osteoarthritis,” Arthritis and Rheumatism, vol. 63, no. 3, pp. 700–707, 2011. View at Publisher · View at Google Scholar · View at Scopus
  120. J. H. Ku, C. K. Lee, B. S. Joo et al., “Correlation of synovial fluid leptin concentrations with the severity of osteoarthritis,” Clinical Rheumatology, vol. 28, no. 12, pp. 1431–1435, 2009. View at Publisher · View at Google Scholar · View at Scopus
  121. C. A. Karvonen-Gutierrez, S. D. Harlow, P. Mancuso, J. Jacobson, C. F. M. de Leon, and B. Nan, “Association of leptin levels with radiographic knee osteoarthritis among a cohort of midlife women,” Arthritis Care and Research, vol. 65, no. 6, pp. 936–944, 2013. View at Publisher · View at Google Scholar
  122. S. Honsawek and M. Chayanupatkul, “Correlation of plasma and synovial fluid adiponectin with knee osteoarthritis severity,” Archives of Medical Research, vol. 41, no. 8, pp. 593–598, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. E. Yusuf, A. Ioan-Facsinay, J. Bijsterbosch et al., “Association between leptin, adiponectin and resistin and long-term progression of hand osteoarthritis,” Annals of the Rheumatic Diseases, vol. 70, no. 7, pp. 1282–1284, 2011. View at Publisher · View at Google Scholar · View at Scopus
  124. M. Filková, M. Lisková, H. Hulejová et al., “Increased serum adiponectin levels in female patients with erosive compared with non-erosive osteoarthritis,” Annals of the Rheumatic Diseases, vol. 68, no. 2, pp. 295–296, 2009. View at Publisher · View at Google Scholar
  125. A. Koskinen, S. Juslin, R. Nieminen, T. Moilanen, K. Vuolteenaho, and E. Moilanen, “Adiponectin associates with markers of cartilage degradation in osteoarthritis and induces production of proinflammatory and catabolic factors through mitogen-activated protein kinase pathways,” Arthritis Research and Therapy, vol. 13, no. 6, article R184, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. J. Y. Choe, J. Bae, H. Y. Jung, S. H. Park, H. J. Lee, and S. K. Kim, “Serum resistin level is associated with radiographic changes in hand osteoarthritis: cross-sectional study,” Joint Bone Spine, vol. 79, no. 2, pp. 160–165, 2012. View at Publisher · View at Google Scholar · View at Scopus
  127. T. N. de Boer, W. E. van Spil, A. M. Huisman et al., “Serum adipokines in osteoarthritis, comparison with controls and relationship with local parameters of synovial inflammation and cartilage damage,” Osteoarthritis and Cartilage, vol. 20, no. 8, pp. 846–853, 2012. View at Publisher · View at Google Scholar