Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 102969, 11 pages
http://dx.doi.org/10.1155/2015/102969
Research Article

Early-Onset Diabetic E1-DN Mice Develop Albuminuria and Glomerular Injury Typical of Diabetic Nephropathy

1Department of Pathology, Haartman Institute, University of Helsinki, Haartmaninkatu 3, 00290 Helsinki, Finland
2Children’s Hospital, University of Helsinki, 00290 Helsinki, Finland
3Department of Pathology, HUSLAB, Helsinki University Central Hospital, 05850 Hyvinkää, Finland
4Department of Pathology, HUSLAB, Helsinki University Central Hospital, 00290 Helsinki, Finland
5Laboratory Animal Centre, University of Helsinki, 00790 Helsinki, Finland
6Biomedicum Stem Cell Center, University of Helsinki, 00290 Helsinki, Finland

Received 8 August 2014; Revised 26 September 2014; Accepted 29 September 2014

Academic Editor: Monica Fedele

Copyright © 2015 Mervi E. Hyvönen 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. G. Pambianco, T. Costacou, D. Ellis, D. J. Becker, R. Klein, and T. J. Orchard, “The 30-year natural history of type 1 diabetes complications: the Pittsburgh epidemiology of diabetes complications study experience,” Diabetes, vol. 55, no. 5, pp. 1463–1469, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. The Diabetes Control and Complications Trial Research Group, “The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependant diabetes mellitus. The diabetes control and complications trial research group,” The New England Journal of Medicine, vol. 329, pp. 977–986, 1993. View at Google Scholar
  3. P. Hovind, L. Tarnow, K. Rossing et al., “Decreasing incidence of severe diabetic microangiopathy in type 1 diabetes,” Diabetes Care, vol. 26, no. 4, pp. 1258–1264, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Borch-Johnsen and S. Kreiner, “Proteinuria: value as predictor of cardiovascular mortality in insulin dependent diabetes mellitus,” British Medical Journal, vol. 294, no. 6588, pp. 1651–1654, 1987. View at Publisher · View at Google Scholar · View at Scopus
  5. P.-H. Groop, M. C. Thomas, J. L. Moran et al., “The presence and severity of chronic kidney disease predicts all-cause mortality in type 1 diabetes,” Diabetes, vol. 58, no. 7, pp. 1651–1658, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Kramer, V. Stel, C. Zoccali et al., “An update on renal replacement therapy in Europe: ERA-EDTA registry data from 1997 to 2006,” Nephrology Dialysis Transplantation, vol. 24, no. 12, pp. 3557–3566, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Ritz, I. Rychlik, F. Locatelli, and S. Halimi, “End-stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions,” The American Journal of Kidney Diseases, vol. 34, no. 5, pp. 795–808, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. G. C. Viberti, R. J. Jarrett, R. D. Hill, A. Argyropoulos, U. Mahmud, and H. Keen, “Microalbuminuria as a predictor of clinical nephropathy in insulin-dependent diabetes mellitus,” The Lancet, vol. 1, no. 8287, pp. 1430–1432, 1982. View at Publisher · View at Google Scholar · View at Scopus
  9. M. L. Caramori, P. Fioretto, and M. Mauer, “The need for early predictors of diabetic nephropathy risk: is albumin excretion rate sufficient?” Diabetes, vol. 49, no. 9, pp. 1399–1408, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Hovind, P. Rossing, L. Tarnow, H. Toft, J. Parving, and H.-H. Parving, “Remission of nephrotic-range albuminuria in type 1 diabetic patients,” Diabetes Care, vol. 24, no. 11, pp. 1972–1977, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. M. E. Molitch, M. Steffes, W. Sun et al., “Development and progression of renal insufficiency with and without albuminuria in adults with type 1 diabetes in the diabetes control and complications trial and the epidemiology of diabetes interventions and complications study,” Diabetes Care, vol. 33, no. 7, pp. 1536–1543, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Fioretto and M. Mauer, “Histopathology of diabetic nephropathy,” Seminars in Nephrology, vol. 27, no. 2, pp. 195–207, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Østeeby, “Morphometric studies of the peripheral glomerular basement membrane in early juvenile diabetes. I. Development of initial basement membrane thickening,” Diabetologia, vol. 8, no. 2, pp. 84–92, 1972. View at Publisher · View at Google Scholar · View at Scopus
  14. S. M. Mauer, M. W. Steffes, E. N. Ellis, D. E. Sutherland, D. M. Brown, and F. C. Goetz, “Structural-functional relationships in diabetic nephropathy,” The Journal of Clinical Investigation, vol. 74, no. 4, pp. 1143–1155, 1984. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Fioretto, M. W. Steffes, D. E. Sutherland, and M. Mauer, “Sequential renal biopsies in insulin-dependent diabetic patients: structural factors associated with clinical progression,” Kidney International, vol. 48, no. 6, pp. 1929–1935, 1995. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Kimmelstiel and C. Wilson, “Intercapillary lesions in the glomeruli of the kidney,” The American Journal of Pathology, vol. 12, no. 1, pp. 83–98, 1936. View at Google Scholar
  17. R. Bader, H. Bader, K. E. Grund, S. Mackensen-Haen, H. Christ, and A. Bohle, “Structure and function of the kidney in diabetic glomerulosclerosis. Correlations between morphological and functional parameters,” Pathology Research and Practice, vol. 167, no. 2–4, pp. 204–216, 1980. View at Publisher · View at Google Scholar · View at Scopus
  18. E. N. Ellis, M. W. Steffes, B. Chavers, and S. M. Mauer, “Observations of glomerular epithelial cell structure in patients with type I diabetes mellitus,” Kidney International, vol. 32, no. 5, pp. 736–741, 1987. View at Publisher · View at Google Scholar · View at Scopus
  19. U. B. Berg, T. B. Torbjörnsdotter, G. Jaremko, and B. Thalme, “Kidney morphological changes in relation to long-term renal function and metabolic control in adolescents with IDDM,” Diabetologia, vol. 41, no. 9, pp. 1047–1056, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. M. W. Steffes, D. Schmidt, R. McCrery et al., “Glomerular cell number in normal subjects and in type 1 diabetic patients,” Kidney International, vol. 59, no. 6, pp. 2104–2113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. M. E. Pagtalunan, P. L. Miller, S. Jumping-Eagle et al., “Podocyte loss and progressive glomerular injury in type II diabetes,” The Journal of Clinical Investigation, vol. 99, no. 2, pp. 342–348, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Toyoda, B. Najafian, Y. Kim, M. L. Caramori, and M. Mauer, “Podocyte detachment and reduced glomerular capillary endothelial fenestration in human type 1 diabetic nephropathy,” Diabetes, vol. 56, no. 8, pp. 2155–2160, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Verzola, M. T. Gandolfo, F. Ferrario et al., “Apoptosis in the kidneys of patients with type II diabetic nephropathy,” Kidney International, vol. 72, no. 10, pp. 1262–1272, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. E. H. Leiter, “Multiple low-dose streptozotocin-induced hyperglycemia and insulitis in C57BL mice: influence of inbred background, sex, and thymus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 2, pp. 630–634, 1982. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Sharma, P. McCue, and S. R. Dunn, “Diabetic kidney disease in the db/db mouse,” American Journal of Physiology—Renal Physiology, vol. 284, no. 6, pp. F1138–F1144, 2003. View at Google Scholar · View at Scopus
  26. J.-H. Chang, S.-Y. Paik, L. Mao et al., “Diabetic kidney disease in FVB/NJ akita mice: temporal pattern of kidney injury and urinary nephrin excretion,” PLoS ONE, vol. 7, no. 4, Article ID e33942, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Zheng, W. T. Noonan, N. S. Metreveli et al., “Development of late-stage diabetic nephropathy in OVE26 diabetic mice,” Diabetes, vol. 53, no. 12, pp. 3248–3257, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. H. J. Zhao, S. Wang, H. Cheng et al., “Endothelial nitric oxide synthase deficiency produces accelerated nephropathy in diabetic mice,” Journal of the American Society of Nephrology, vol. 17, no. 10, pp. 2664–2669, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. M. D. Breyer, E. Böttinger, F. C. Brosius III et al., “Mouse models of diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 16, no. 1, pp. 27–45, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. C. E. Alpers and K. L. Hudkins, “Mouse models of diabetic nephropathy,” Current Opinion in Nephrology and Hypertension, vol. 20, no. 3, pp. 278–284, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. P. J. Miettinen, J. Ustinov, P. Ormio et al., “Downregulation of EGF receptor signaling in pancreatic islets causes diabetes due to impaired postnatal β-cell growth,” Diabetes, vol. 55, no. 12, pp. 3299–3308, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Hakonen, J. Ustinov, I. Mathijs et al., “Epidermal growth factor (EGF)-receptor signalling is needed for murine beta cell mass expansion in response to high-fat diet and pregnancy but not after pancreatic duct ligation,” Diabetologia, vol. 54, no. 7, pp. 1735–1743, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. M. E. Hyvönen, P. Saurus, A. Wasik et al., “Lipid phosphatase SHIP2 downregulates insulin signalling in podocytes,” Molecular and Cellular Endocrinology, vol. 328, no. 1-2, pp. 70–79, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Østerby, H. J. G. Gundersen, G. Nyberg, and M. Aurell, “Advanced diabetic glomerulopathy: quantitative structural characterization of nonoccluded glomeruli,” Diabetes, vol. 36, no. 5, pp. 612–619, 1987. View at Publisher · View at Google Scholar · View at Scopus
  35. J. G. van den Berg, M. A. van den Bergh Weerman, K. J. M. Assmann, J. J. Weening, and S. Florquin, “Podocyte foot process effacement is not correlated with the level of proteinuria in human glomerulopathies,” Kidney International, vol. 66, no. 5, pp. 1901–1906, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. D. M. Nathan, B. Zinman, P. A. Cleary, and et al, “Modern-day clinical course of type 1 diabetes mellitus after 30 years' duration: the diabetes control and complications trial/epidemiology of diabetes interventions and complications and Pittsburgh epidemiology of diabetes complications experience (1983–2005),” Archives of Internal Medicine, vol. 169, no. 14, pp. 1307–1316, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Reichard, M. Pihl, U. Rosenqvist, and J. Sule, “Complications in IDDM are caused by elevated blood glucose level: the Stockholm Diabetes Intervention Study (SDIS) at 10-year follow up,” Diabetologia, vol. 39, no. 12, pp. 1483–1488, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Brownlee, “Biochemistry and molecular cell biology of diabetic complications,” Nature, vol. 414, no. 6865, pp. 813–820, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Okada, T. Nagao, H. Matsumoto, Y. Nagaoka, T. Wada, and T. Nakao, “Histological predictors for renal prognosis in diabetic nephropathy in diabetes mellitus type 2 patients with overt proteinuria,” Nephrology, vol. 17, no. 1, pp. 68–75, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Rasch and J. O. R. Nörgaard, “Renal enlargement: comparative autoradiographic studies of 3H-thymidine uptake in diabetic and uninephrectomized rats,” Diabetologia, vol. 25, no. 3, pp. 280–287, 1983. View at Publisher · View at Google Scholar · View at Scopus
  41. M. S. Mozaffari, R. Abdelsayed, J. Y. Liu, I. Zakhary, and B. Baban, “Renal distal tubule proliferation and increased aquaporin 2 level but decreased urine osmolality in db/db mouse: treatment with chromium picolinate,” Experimental and Molecular Pathology, vol. 92, no. 1, pp. 54–58, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Menini, C. Iacobini, G. Oddi et al., “Increased glomerular cell (podocyte) apoptosis in rats with streptozotocin-induced diabetes mellitus: role in the development of diabetic glomerular disease,” Diabetologia, vol. 50, no. 12, pp. 2591–2599, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Susztak, A. C. Raff, M. Schiffer, and E. P. Böttinger, “Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy,” Diabetes, vol. 55, no. 1, pp. 225–233, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. E. Grishman and J. Churg, “Focal glomerular sclerosis in nephrotic patients: an electron microscopic study of glomerular podocytes,” Kidney International, vol. 7, no. 2, pp. 111–122, 1975. View at Publisher · View at Google Scholar · View at Scopus
  45. W. Kriz, N. Gretz, and K. V. Lemley, “Progression of glomerular diseases: is the podocyte the culprit?” Kidney International, vol. 54, no. 3, pp. 687–697, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Menne, M. Meier, J.-K. Park et al., “Nephrin loss in experimental diabetic nephropathy is prevented by deletion of protein kinase C alpha signaling in-vivo,” Kidney International, vol. 70, no. 8, pp. 1456–1462, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Doublier, G. Salvidio, E. Lupia et al., “Nephrin expression is reduced in human diabetic nephropathy: evidence for a distinct role for glycated albumin and angiotensin II,” Diabetes, vol. 52, no. 4, pp. 1023–1030, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Langham, D. Kelly, A. Cox et al., “Proteinuria and the expression of the podocyte slit diaphragm protein, nephrin, in diabetic nephropathy: effects of angiotensin converting enzyme inhibition,” Diabetologia, vol. 45, no. 11, pp. 1572–1576, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Benigni, E. Gagliardini, S. Tomasoni et al., “Selective impairment of gene expression and assembly of nephrin in human diabetic nephropathy,” Kidney International, vol. 65, no. 6, pp. 2193–2200, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. S. B. Gurley, C. L. Mach, J. Stegbauer et al., “Influence of genetic background on albuminuria and kidney injury in Ins2(+/C96Y) (Akita) mice,” American Journal of Physiology: Renal Physiology, vol. 298, no. 3, pp. F788–F795, 2010. View at Google Scholar