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Journal of Diabetes Research
Volume 2016, Article ID 2315260, 8 pages
http://dx.doi.org/10.1155/2016/2315260
Research Article

Association of Haemostatic and Inflammatory Biomarkers with Nephropathy in Type 1 Diabetes Mellitus

1Departamento de Analises Clínicas e Toxicológicas, Faculdade de Farmácia, Universidade Federal de São João Del-Rei, Campus Centro Oeste Dona Lindu, 35501-296 Divinopolis, MG, Brazil
2Departamento de Clínica Médica, Faculdade de Medicina, Universidade Federal de Minas Gerais, 30130-100 Belo Horizonte, MG, Brazil
3Departamento de Endocrinologia e Metabolismo, Instituto de Educação e Pesquisa da Santa Casa de Belo Horizonte, 30150-250 Belo Horizonte, MG, Brazil
4Departamento de Analises Clínicas e Toxicológicas, Faculdade de Farmácia, Universidade Federal de Minas Gerais, 31270-901 Belo Horizonte, MG, Brazil

Received 19 May 2015; Accepted 4 August 2015

Academic Editor: David W. Powell

Copyright © 2016 Caroline Pereira Domingueti 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.-I. Yamagishi and T. Matsui, “Advanced glycation end products, oxidative stress and diabetic nephropathy,” Oxidative Medicine and Cellular Longevity, vol. 3, no. 2, pp. 101–108, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. National Disease: Improving Global Outcomes (KDIGO) CKD Work Group, “KDIGO clinical practive guideline for the evaluation and management of chronic kidney disease,” Kidney International Supplements, vol. 3, pp. 1–150, 2013. View at Google Scholar
  3. K. Kanasaki, G. Taduri, and D. Koya, “Diabetic nephropathy: the role of inflammation in fibroblast activation and kidney fibrosis,” Frontiers in Endocrinology, vol. 4, article 7, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. M. B. Duran-Salgado and A. F. Rubio-Guerra, “Diabetic nephropathy and inflammation,” World Journal of Diabetes, vol. 5, pp. 393–398, 2014. View at Google Scholar
  5. J. F. Navarro-González, C. Mora-Fernández, M. M. De Fuentes, and J. García-Pérez, “Inflammatory molecules and pathways in the pathogenesis of diabetic nephropathy,” Nature Reviews Nephrology, vol. 7, no. 6, pp. 327–340, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. R. B. Goldberg, “Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications,” The Journal of Clinical Endocrinology & Metabolism, vol. 94, no. 9, pp. 3171–3182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Trifunović, L. Miller, Ž. Debeljak, and V. Horvat, “Pathologic patterns of interleukin 10 expression—a review,” Biochemia Medica, vol. 25, no. 1, pp. 36–48, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Kessler, M. L. Wiesel, P. Attali, J. M. Mossard, J. P. Cazenave, and M. Finget, “Von willebrand factor in diabetic angiopathy,” Diabetes and Metabolism, vol. 24, no. 4, pp. 327–336, 1998. View at Google Scholar · View at Scopus
  9. N. N. Chan, J. H. Fuller, M. Rubens, and H. M. Colhoun, “Von Willebrand factor in type 1 diabetes: its relationship with endothelial nitric oxide production and coronary artery calcification,” Medical Science Monitor, vol. 9, no. 7, pp. CR297–CR303, 2003. View at Google Scholar · View at Scopus
  10. P. V. Jenkins and J. S. O'Donnell, “ABO blood group determines plasma von Willebrand factor levels: a biologic function after all?” Transfusion, vol. 46, no. 10, pp. 1836–1844, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. M. A. El.Asrar, A. A. Adly, E. S. El Hadidy, and M. A. Abdelwahab, “D-dimer levels in type 1 and type 2 diabetic children and adolescents; relation to microvascular complications and dyslipidemia “own data and review”,” Pediatric Endocrinology Reviews, vol. 9, no. 3, pp. 657–668, 2012. View at Google Scholar · View at Scopus
  12. Z. F. Long, G. Y. Qu, and M. Xu, “Relationship between the level of plasma D-dimer and diabetic microangiopathy,” Hunan Yi Ke Da Xue Xue Bao, vol. 26, no. 5, pp. 434–436, 2001. View at Google Scholar · View at Scopus
  13. C. P. Domingueti, L. M. S. Dusse, M. D. G. Carvalho, K. B. Gomes, and A. P. Fernandes, “Hypercoagulability and cardiovascular disease in diabetic nephropathy,” Clinica Chimica Acta, vol. 415, pp. 279–285, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. C. P. Domingueti, L. M. Dusse, R. B. Fóscolo et al., “Von Willebrand factor, ADAMTS13 and D-Dimer are correlated with different levels of nephropathy in type 1 diabetes mellitus,” PLoS ONE, vol. 10, no. 7, Article ID e0132784, 2015. View at Publisher · View at Google Scholar
  15. American Diabetes Association, “Standards of medical care in diabetes,” Diabetes Care, vol. 38, pp. S1–S94, 2015. View at Google Scholar
  16. A. S. Levey, L. A. Stevens, C. H. Schmid et al., “A new equation to estimate glomerular filtration rate,” Annals of Internal Medicine, vol. 150, no. 9, pp. 604–612, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Zhang, C. Xiao, P. Wang et al., “The alteration of Th1/Th2/Th17/Treg paradigm in patients with type 2 diabetes mellitus: relationship with diabetic nephropathy,” Human Immunology, vol. 75, no. 4, pp. 289–296, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Nosratabadi, M. K. Arababadi, G. Hassanshahi et al., “Evaluation of IFN-γ serum level in nephropatic type 2 diabetic patients,” Pakistan Journal of Biological Sciences, vol. 12, no. 9, pp. 746–749, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Shelbaya, H. Amer, S. Seddik et al., “Study of the role of interleukin-6 and highly sensitive C-reactive protein in diabetic nephropathy in type 1 diabetic patients,” European Review for Medical and Pharmacological Sciences, vol. 16, no. 2, pp. 176–182, 2012. View at Google Scholar · View at Scopus
  20. K. Sahakyan, B. E. K. Klein, K. E. Lee, M. Y. Tsai, and R. Klein, “Inflammatory and endothelial dysfunction markers and proteinuria in persons with type 1 diabetes mellitus,” European Journal of Endocrinology, vol. 162, no. 6, pp. 1101–1105, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. M. T. Schram, N. Chaturvedi, C. G. Schalkwijk, J. H. Fuller, and C. D. A. Stehouwer, “Markers of inflammation are cross-sectionally associated with microvascular complications and cardiovascular disease in type 1 diabetes—the EURODIAB Prospective Complications Study,” Diabetologia, vol. 48, no. 2, pp. 370–378, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Saraheimo, A.-M. Teppo, C. Forsblom, J. Fagerudd, and P.-H. Groop, “Diabetic nephropathy is associated with low-grade inflammation in type 1 diabetic patients,” Diabetologia, vol. 46, no. 10, pp. 1402–1407, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Ramakrishnan, P. M. Clark, D. E. Mason, E. C. Peters, L. C. Hsieh-Wilson, and D. Baltimore, “Activation of the transcriptional function of the NF-kB protein c-Rel by O-GlcNAc glycosylation,” Science Signaling, vol. 6, no. 290, article ra75, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Giannini, A. Mohn, F. Chiarelli, and C. J. H. Kelnar, “Macrovascular angiopathy in children and adolescents with type 1 diabetes,” Diabetes/Metabolism Research and Reviews, vol. 27, no. 5, pp. 436–460, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Hasegawa, K. Nakano, M. Sawada et al., “Possible role of tumor necrosis factor and interleukin-1 in the development of diabetic nephropathy,” Kidney International, vol. 40, no. 6, pp. 1007–1012, 1991. View at Publisher · View at Google Scholar · View at Scopus
  26. C.-C. Wu, J.-S. Chen, K.-C. Lu et al., “Aberrant cytokines/chemokines production correlate with proteinuria in patients with overt diabetic nephropathy,” Clinica Chimica Acta, vol. 411, no. 9-10, pp. 700–704, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Matoba, D. Kawanami, S. Ishizawa, Y. Kanazawa, T. Yokota, and K. Utsunomiya, “Rho-kinase mediates TNF-α-induced MCP-1 expression via p38 MAPK signaling pathway in mesangial cells,” Biochemical and Biophysical Research Communications, vol. 402, no. 4, pp. 725–730, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Mohamed, C. Jayakumar, and G. Ramesh, “Chronic administration of EP4-selective agonist exacerbates albuminuria and fibrosis of the kidney in streptozotocin-induced diabetic mice through IL-6,” Laboratory Investigation, vol. 93, no. 8, pp. 933–945, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Margetic, “Inflammation and haemostasis,” Biochemia Medica, vol. 22, no. 1, pp. 49–62, 2012. View at Google Scholar · View at Scopus
  30. P. P. Wolkow, M. A. Niewczas, B. Perkins et al., “Association of urinary inflammatory markers and renal decline in microalbuminuric type 1 diabetics,” Journal of the American Society of Nephrology, vol. 19, no. 4, pp. 789–797, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. E. Hellemons, J. Kerschbaum, S. J. L. Bakker et al., “Validity of biomarkers predicting onset or progression of nephropathy in patients with type 2 diabetes: a systematic review,” Diabetic Medicine, vol. 29, no. 5, pp. 567–577, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Wu, Y. Ding, C. Zhu et al., “Urinary TNF-α and NGAL are correlated with the progression of nephropathy in patients with type 2 diabetes,” Experimental and Therapeutic Medicine, vol. 6, no. 6, pp. 1482–1488, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. M. A. Niewczas, T. Gohda, J. Skupien et al., “Circulating TNF receptors 1 and 2 predict ESRD in type 2 diabetes,” Journal of the American Society of Nephrology, vol. 23, no. 3, pp. 507–515, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Myśliwska, K. Zorena, E. Semetkowska-Jurkiewicz, D. Rachón, H. Suchanek, and A. Myśliwski, “High levels of circulating interleukin-10 in diabetic nephropathy patients,” European Cytokine Network, vol. 16, no. 2, pp. 117–122, 2005. View at Google Scholar · View at Scopus
  35. X. R. Huang, A. R. Kitching, P. G. Tipping, and S. R. Holdsworth, “Interleukin-10 inhibits macrophage-induced glomerular injury,” Journal of the American Society of Nephrology, vol. 11, no. 2, pp. 262–269, 2000. View at Google Scholar · View at Scopus
  36. K. F. Rodrigues, N. T. Pietrani, V. C. Sandrim et al., “Association of a large panel of cytokine gene polymorphisms with complications and comorbidities in type 2 diabetes patients,” Journal of Diabetes Research, vol. 2015, Article ID 605965, 9 pages, 2015. View at Publisher · View at Google Scholar
  37. C. D. A. Stehouwer, E. S. G. Stroes, W. H. L. Hackeng, P. G. H. Mulder, and G. J. H. Den Ottolander, “Von Willebrand factor and development of diabetic nephropathy in IDDM,” Diabetes, vol. 40, no. 8, pp. 971–976, 1991. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Holzinger, E. Weissinger, A. Zuckermann et al., “Effects of interleukin-1, -2, -4, -6, interferon-gamma and granulocyte/macrophage colony stimulating factor on human vascular endothelial cells,” Immunology Letters, vol. 35, no. 2, pp. 109–117, 1993. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Oggianu, S. Lancellotti, D. Pitocco et al., “The oxidative modification of von Willebrand factor is associated with thrombotic angiopathies in diabetes mellitus,” PLoS ONE, vol. 8, no. 1, Article ID e55396, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Bernardo, C. Ball, L. Nolasco, J. F. Moake, and J.-F. Dong, “Effects of inflammatory cytokines on the release and cleavage of the endothelial cell-derived ultralarge von Willebrand-factor multimers under flow,” Blood, vol. 104, no. 1, pp. 100–106, 2004. View at Publisher · View at Google Scholar · View at Scopus