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International Journal of Endocrinology
Volume 2017, Article ID 8724869, 8 pages
https://doi.org/10.1155/2017/8724869
Research Article

Serum Osteoprotegerin Is a Potential Biomarker of Insulin Resistance in Chinese Postmenopausal Women with Prediabetes and Type 2 Diabetes

1Department of Endocrinology and Metabolism, Nanchang Key Laboratory of Diabetes, The Third Hospital of Nanchang, No. 2 Xiangshan South Road, Nanchang, Jiangxi 330009, China
2Department of Finance, Nanchang Normal University, No. 889 Ruixiang Road, Nanchang, Jiangxi 330009, China

Correspondence should be addressed to Ping Tu; moc.621@7788gniput

Received 21 August 2016; Revised 28 October 2016; Accepted 14 November 2016; Published 31 January 2017

Academic Editor: Andre Pascal Kengne

Copyright © 2017 Peng Duan 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. T. J. Martin and N. A. Sims, “RANKL/OPG; critical role in bone physiology,” Reviews in Endocrine & Metabolic Disorders, vol. 16, no. 2, pp. 131–139, 2015. View at Google Scholar
  2. W. Liu and X. Zhang, “Receptor activator of nuclear factor-κB ligand (RANKL)/RANK/osteoprotegerin system in bone and other tissues,” Molecular Medicine Reports, vol. 11, no. 5, pp. 3212–3218, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Augoulea, N. Vrachnis, I. Lambrinoudaki et al., “Osteoprotegerin as a marker of atherosclerosis in diabetic patients,” International Journal of Endocrinology, vol. 2013, Article ID 182060, 6 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Esteghamati, M. Aflatoonian, M. V. Rad et al., “Association of osteoprotegerin with peripheral artery disease in patients with type 2 diabetes,” Archives of Cardiovascular Diseases, vol. 108, no. 8, pp. 412–419, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Pérez de Ciriza, A. Lawrie, and N. Varo, “Osteoprotegerin in cardiometabolic disorders,” International Journal of Endocrinology, vol. 2015, Article ID 564934, 15 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. J. R. Lewis, W. H. Lim, T. Ueland et al., “Elevated circulating osteoprotegerin and renal dysfunction predict 15-year cardiovascular and all-cause mortality: a prospective study of elderly Women,” PLoS ONE, vol. 10, no. 7, Article ID e0134266, 2015. View at Publisher · View at Google Scholar
  7. T. Morisawa, A. Nakagomi, K. Kohashi et al., “Osteoprotegerin is associated with endothelial function and predicts early carotid atherosclerosis in patients with coronary artery disease,” International Heart Journal, vol. 56, no. 6, pp. 605–612, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. I. Lambrinoudaki, E. Tsouvalas, M. Vakaki et al., “Osteoprotegerin, soluble receptor activator of nuclear factor-κB ligand, and subclinical atherosclerosis in children and adolescents with type 1 diabetes mellitus,” International Journal of Endocrinology, vol. 2013, Article ID 102120, 8 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. A. M. Blázquez-Medela, J. M. López-Novoa, and C. Martínez-Salgado, “Osteoprotegerin and diabetes-associated pathologies,” Current Molecular Medicine, vol. 11, no. 5, pp. 401–416, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Tu, P. Duan, R. S. Zhang et al., “Polymorphisms in genes in the RANKL/RANK/OPG pathway are associated with bone mineral density at different skeletal sites in post-menopausal women,” Osteoporosis International, vol. 26, no. 1, pp. 179–185, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. R. E. Maser, M. J. Lenhard, M. B. Sneider, and R. T. Pohlig, “Osteoprotegerin is a better serum biomarker of coronary artery calcification than osteocalcin in type 2 diabetes,” Endocrine Practice, vol. 21, no. 1, pp. 14–22, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. D. R. Matthews, J. P. Hosker, A. S. Rudenski, B. A. Naylor, D. F. Treacher, and R. C. Turner, “Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man,” Diabetologia, vol. 28, no. 7, pp. 412–419, 1985. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Katz, S. S. Nambi, K. Mather et al., “Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans,” The Journal of Clinical Endocrinology & Metabolism, vol. 85, no. 7, pp. 2402–2410, 2000. View at Publisher · View at Google Scholar
  14. A. S. Levey, J. P. Bosch, J. B. Lewis, T. Greene, N. Rogers, and D. Roth, “A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group,” Annals of Internal Medicine, vol. 130, no. 6, pp. 461–470, 1999. View at Publisher · View at Google Scholar
  15. Y. Li, K. Wang, Q. Y. Zou, R. R. Magness, and J. Zheng, “2,3,7,8-Tetrachlorodibenzo-p-dioxin differentially suppresses angiogenic responses in human placental vein and artery endothelial cells,” Toxicology, vol. 336, pp. 70–78, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. A. F. Cicero, M. Rosticci, A. Parini et al., “Short-term effects of a combined nutraceutical of insulin-sensitivity, lipid level and indexes of liver steatosis: a double-blind, randomized, cross-over clinical trial,” Nutrition Journal, vol. 2015, no. 14, article 30, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Esteghamati, H. Ashraf, A. R. Esteghamati et al., “Optimal threshold of homeostasis model assessment for insulin resistance in an Iranian population: the implication of metabolic syndrome to detect insulin resistance,” Diabetes Research and Clinical Practice, vol. 84, no. 3, pp. 279–287, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Gayoso-Diz, A. Otero-González, M. X. Rodriguez-Alvarez, F. García, A. De Francisco, and A. G. Quintela, “Insulin resistance (HOMA-IR) cut-off values and the metabolic syndrome in a general adult population: effect of gender and age: EPIRCE cross-sectional study,” BMC Endocrine Disorders, vol. 2013, no. 13, article 47, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Yaturu, J. Rains, and S. K. Jain, “Relationship of elevated osteoprotegerin with insulin resistance, CRP, and TNF-alpha levels in men with type 2 diabetes,” Cytokine, vol. 44, no. 1, pp. 168–171, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. H. Gannagé-Yared, C. Yaghi, B. Habre et al., “Osteoprotegerin in relation to body weight, lipid parameters, insulin sensitivity, adipocytokines, and C-reactive protein in obese and non-obese young individuals: results from both cross-sectional and interventional study,” European Journal of Endocrinology, vol. 158, no. 3, pp. 353–359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. C. N. Ayina Ayina, E. Sobngwi, M. Essouma et al., “Osteoprotegerin in relation to insulin resistance and blood lipids in sub-Saharan African women with and without abdominal obesity,” Diabetology & Metabolic Syndrome, vol. 2015, no. 7, article 47, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Ugur-Altun, A. Altun, M. Gerenli, and A. Tugrul, “The relationship between insulin resistance assessed by HOMA-IR and serum osteoprotegerin levels in obesity,” Diabetes Research and Clinical Practice, vol. 68, no. 3, pp. 217–222, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. E. S. Oh, E. J. Rhee, K. W. Oh et al., “Circulating osteoprotegerin levels are associated with age, waist-to-hip ratio, serum total cholesterol, and low-density lipoprotein cholesterol levels in healthy Korean women,” Metabolism, vol. 54, no. 1, pp. 49–54, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. E. P. O’Sullivan, D. T. Ashley, C. Davenport et al., “A comparison of osteoprotegerin with adiponectin and high-sensitivity C-reactive protein (hsCRP) as a marker for insulin resistance,” Metabolism, vol. 54, no. 1, pp. 34–38, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Niu, Z. Yang, X. Li, and W. ZhangS. Lu, H. Zhang, X. Chen et al., “Association of osteoprotegerin with impaired glucose regulation and microalbuminuria: the REACTION study,” BMC Endocrine Disorders, vol. 2015, no. 15, article 75, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. H. H. Wang and G. D. Xiang, “Changes of plasma concentration of osteoprotegerin and its association with endothelial dysfunction before and after hypouricemic therapy in patients with hyperuricemia,” Modern Rheumatology, vol. 25, no. 1, pp. 123–127, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Z. Jiang, K. Wang, Y. Li et al., “Enhanced cellular responses and distinct gene profiles in human fetoplacental artery endothelial cells under chronic low oxygen,” Biology of Reproduction, vol. 89, no. 6, article 133, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Z. Jiang, K. Wang, Y. Li et al., “Transcriptional and functional adaptations of human endothelial cells to physiological chronic low oxygen,” Biology of Reproduction, vol. 88, no. 5, article 114, 2013. View at Publisher · View at Google Scholar
  29. Y. Z. Jiang, Y. Li, K. Wang et al., “Distinct roles of HIF1A in endothelial adaptations to physiological and ambient oxygen,” Molecular and Cellular Endocrinology, vol. 391, no. 1, pp. 60–67, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. J. S. McGonigle, C. M. Giachelli, and M. Scatena, “Osteoprotegerin and RANKL differentially regulate angiogenesis and endothelial cell function,” Angiogenesis, vol. 12, no. 1, pp. 35–46, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. S. T. Wang, C. Y. Zhang, C. M. Zhang, C. M. Zhang, and W. Rong, “The plasma osteoprotegerin level and osteoprotegerin expression in renal biopsy tissue are increased in type 2 diabetes with nephropathy,” Experimental and Clinical Endocrinology & Diabetes, vol. 123, no. 2, pp. 106–111, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Secchiero, F. Corallini, A. Pandolfi et al., “An increased osteoprotegerin serum release characterizes the early onset of diabetes mellitus and may contribute to endothelial cell dysfunction,” The American Journal of Pathology, vol. 169, no. 6, pp. 2236–2244, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Chen, R. Chen, H. Wang, and F. Liang, “Mechanisms linking inflammation to insulin resistance,” International Journal of Endocrinology, vol. 2015, Article ID 508409, 9 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Bernardi, B. Fabris, M. Thomas et al., “Osteoprotegerin increases in metabolic syndrome and promotes adipose tissue proinflammatory changes,” Molecular and Cellular Endocrinology, vol. 394, no. 1, pp. 13–20, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Shimamura, H. Nakagami, M. K. Osako et al., “OPG/RANKL/RANK axis is a critical inflammatory signaling system in ischemic brain in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 22, pp. 8191–8196, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. N. G. Kondegowda, R. Fenutria, I. R. Pollack et al., “Osteoprotegerin and denosumab stimulate human beta cell proliferation through inhibition of the receptor activator of NF-κB ligand pathway,” Cell Metabolism, vol. 22, no. 1, pp. 77–85, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Weidemann, A. Lovas, A. Rauch et al., “Classical and alternative NF-κB signaling cooperate in regulating adipocyte differentiation and function,” International Journal of Obesity, vol. 40, no. 3, pp. 452–459, 2016. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Kiechl, J. Wittmann, A. Giaccari et al., “Blockade of receptor activator of nuclear factor-κB (RANKL) signaling improves hepatic insulin resistance and prevents development of diabetes mellitus,” Nature Medicine, vol. 19, no. 3, pp. 358–363, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. M. B. Loureiro, M. A. Ururahy, F. P. Freire-Neto et al., “Low bone mineral density is associated to poor glycemic control and increased OPG expression in children and adolescents with type 1 diabetes,” Diabetes Research and Clinical Practice, vol. 103, no. 3, pp. 452–457, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Suzuki, T. Kurose, M. Takizawa et al., “Osteoclastic function is accelerated in male patients with type 2 diabetes mellitus: the preventive role of osteoclastogenesis inhibitory factor/osteoprotegerin (OCIF/OPG) on the decrease of bone mineral density,” Diabetes Research and Clinical Practice, vol. 68, no. 2, pp. 117–125, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Nabipour, B. Larijani, K. Vahdat et al., “Relationships among serum receptor of nuclear factor-kappaB ligand, osteoprotegerin, high-sensitivity C-reactive protein, and bone mineral density in postmenopausal women: osteoimmunity versus osteoinflammatory,” Menopause, vol. 16, no. 5, pp. 950–955, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Kudlacek, B. Schneider, W. Woloszczuk, P. Pietschmann, R. Willvonseder, and Austrian Study Group on Normative Values of Bone Metabolism, “Serum levels of osteoprotegerin increase with age in a healthy adult population,” Bone, vol. 32, no. 6, pp. 681–686, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. A. E. Altinova, F. Toruner, M. Akturk et al., “Relationship between serum osteoprotegerin, glycemic control, renal function and markers of atherosclerosis in type 2 diabetes,” Scandinavian Journal of Clinical and Laboratory Investigation, vol. 71, no. 4, pp. 340–343, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Khosla, H. M. Arrighi, L. J. Melton et al., “Correlates of osteoprotegerin levels in women and men,” Osteoporosis International, vol. 13, no. 5, pp. 394–399, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. A. R. Moschen, A. Kaser, S. Stadlmann et al., “The RANKL/OPG system and bone mineral density in patients with chronic liver disease,” Journal of Hepatology, vol. 43, no. 6, pp. 973–983, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Shaarawy, S. A. Fathy, N. L. Mehany, and O. W. Hindy, “Circulating levels of osteoprotegerin and receptor activator of NF-kappaB ligand in patients with chronic renal failure,” Clinical Chemistry and Laboratory Medicine, vol. 45, no. 11, pp. 1498–1503, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Spartalis and A. Papagianni, “Receptor activator of nuclear factor κB ligand/osteoprotegerin axis and vascular calcifications in patients with chronic kidney disease,” World Journal of Nephrology, vol. 5, no. 1, pp. 1–5, 2016. View at Publisher · View at Google Scholar