Podocyte injury in diabetes mellitus
Abstract
The mechanisms of podocyte injury and their correlation with metabolic and haemodynamic disorders in diabetes mellitus are considered in detail; the results of the last experimental and clinical studies on this problem are presented in this review. Authors shined the biomarkers, reflecting expressiveness of podocytopathy and structural and functional glomerular changes at diabetic nephropathy. Modern possibilities of treatment for their correction to prevent diabetic nephropathy progression are discussed.
About the Authors
Irina Nikolaevna Bobkova
Sechenov First Moscow State Medical University, Moscow
Russian Federation
MD, PhD, Professor, Department of nephrology and hemodialysis of the Institute of professional education
Russian Federation
MD, PhD, Professor, Department of nephrology and hemodialysis of the Institute of professional education
Marina Vladimirovna Shestakova
Endocrinology Research Centre, Moscow
Russian Federation
Russian Federation
MD, PhD, Member of Russian Academy of Sciences
Head of the Diabetes Institute, Endocrinology Research Centre
Head of the Endocrinology and Diabetology Department, Sechenov First Moscow State Medical UniversityAnna Alexandrovna Shchukina
Sechenov First Moscow State Medical University, Moscow
Russian Federation
Graduate student, department of nephrology and hemodialysis of Institute of professional education
Russian Federation
Graduate student, department of nephrology and hemodialysis of Institute of professional education
References
1. Dedov II. Diabetes mellitus: development of technologies in diagnostics, treatment and prevention. Diabetes mellitus 2010; (3):6-13. Available from: http://endojournals.ru/index.php/dia/article/view/5480 doi: 10.14341/2072-0351-5480
2. Shamkhalova MS, Trubitsyna NP, Shestakova MV. New prospects in the treatment of diabetes mellitus. Diabetes mellitus 2012; (4):109-114. Available from: http://endojournals.ru/index.php/dia/article/view/5547 doi: 10.14341/2072-0351-5547
3. Lebedeva NO, Vikulova OK. Pre-clinical markers for diagnosis of diabetic nephropathy in patients with type 1 diabetes mellitus. Diabetes mellitus 2012; (2):38-45. Available from: http://endojournals.ru/index.php/dia/article/view/5517 doi: 10.14341/2072-0351-5517
4. IDF Diabetes Atlas. 6-th edition. 2013. Available from: http://www.idf.org/diabetesatlas.
5. Dedov II, Shestakova MV. Diabetes mellitus and Chronic kidney desease. Moscow: Medical news Agency; 2009.
6. Shestakova MV, Shamkhalova MS, Yarek-Martynova IY, Klefortova II, Sukhareva OY, Vikulova OK, et al. Diabetes mellitus and chronic kidney disease: achievements, unresolved problems, and prospects for therapy. Diabetes mellitus 2011; (1):81-88. Available from: http://endojournals.ru/index.php/dia/article/view/6254 doi: 10.14341/2072-0351-6254
7. Granier C, Makni K, Molina L, Jardin-Watelet B, Ayadi H, Jarraya F. Gene and protein markers of diabetic nephropathy. Nephrology Dialysis Transplantation 2007;23(3):792-799. Available from: http://ndt.oxfordjournals.org/cgi/doi/10.1093/ndt/gfm834 doi: 10.1093/ndt/gfm834
8. Caramori ML, Fioretto P, Mauer M. The need for early predictors of diabetic nephropathy risk: is albumin excretion rate sufficient. Diabetes 2000;49(9):1399-1408. Available from: http://diabetes.diabetesjournals.org/cgi/doi/10.2337/diabetes.49.9.1399 PubMed PMID: 10969821. doi: 10.2337/diabetes.49.9.1399
9. Shankland SJ. The podocyte's response to injury: Role in proteinuria and glomerulosclerosis. Kidney Int 2006;69(12):2131-2147. Available from: http://www.nature.com/doifinder/10.1038/sj.ki.5000410 doi: 10.1038/sj.ki.5000410
10. Duval CW, Aunoy, R. D' . STUDIES UPON EXPERIMENTAL MEASLES : I. THE EFFECTS OF THE VIRUS OF MEASLES UPON THE GUINEA PIG. J Exp Med 1922;35(2):257-270. Available from: http://jem.rupress.org/cgi/pmidlookup?view=long&pmid=19868603 PubMed PMID: 19868603
11. Stitt-Cavanagh E, MacLoed L, Kennedy CRJ. The Podocyte in Diabetic Kidney Disease. The Scientific World JOURNAL 2009;9:1127-1139. Available from: http://www.hindawi.com/journals/tswj/2009/692670/abs PubMed PMID: 19838599. doi: 10.1100/tsw.2009.133
12. Reddy GR, Kotlyarevska K, Ransom RF, Menon RK. The podocyte and diabetes mellitus: is the podocyte the key to the origins of diabetic nephropathy. Current Opinion in Nephrology and Hypertension 2008;17(1):32-36. Available from: http://content.wkhealth.com/linkback/openurl?sid=WKPTLP:landingpage&an=00041552-200801000-00006 PubMed PMID: 18090667. doi: 10.1097/MNH.0b013e3282f2904d
13. Wolf G, Chen S, Ziyadeh FN. From the Periphery of the Glomerular Capillary Wall Toward the Center of Disease: Podocyte Injury Comes of Age in Diabetic Nephropathy. Diabetes 2005;54(6):1626-1634. Available from: http://diabetes.diabetesjournals.org/cgi/doi/10.2337/diabetes.54.6.1626 PubMed PMID: 15919782. doi: 10.2337/diabetes.54.6.1626
14. Ziyadeh F, Wolf G. Pathogenesis of the Podocytopathy and Proteinuria in Diabetic Glomerulopathy. CDR 2008;4(1):39-45. Available from: http://www.eurekaselect.com/openurl/content.php?genre=article&issn=1573-3998&volume=4&issue=1&spage=39 doi: 10.2174/157339908783502370
15. Steffes MW, Schmidt D, Mccrery R, Basgen JM, Group IDN. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 2001;59(6):2104-2113. Available from: http://www.nature.com/doifinder/10.1046/j.1523-1755.2001.00725.x doi: 10.1046/j.1523-1755.2001.00725.x
16. Patari A, Forsblom C, Havana M, Taipale H, Groop PH, Holthofer H. Nephrinuria in Diabetic Nephropathy of Type 1 Diabetes. Diabetes 2003;52(12):2969-2974. Available from: http://diabetes.diabetesjournals.org/cgi/doi/10.2337/diabetes.52.12.2969 PubMed PMID: 14633858. doi: 10.2337/diabetes.52.12.2969
17. Lewko B, Stepinski J. Hyperglycemia and mechanical stress: Targeting the renal podocyte. J. Cell. Physiol 2009;221(2):288-295. Available from: http://doi.wiley.com/10.1002/jcp.21856 PubMed PMID: 19562677. doi: 10.1002/jcp.21856
18. Diez-Sampedro A, Lenz O, Fornoni A. Podocytopathy in Diabetes: A Metabolic and Endocrine Disorder. American Journal of Kidney Diseases 2011;58(4):637-646. Available from: http://linkinghub.elsevier.com/retrieve/pii/S027263861100919X PubMed PMID: 21719174. doi: 10.1053/j.ajkd.2011.03.035
19. Dalla Vestra M , Masiero A, Roiter AM, Saller A, Crepaldi G, Fioretto P. Is Podocyte Injury Relevant in Diabetic Nephropathy?: Studies in Patients With Type 2 Diabetes. Diabetes 2003;52(4):1031-1035. Available from: http://diabetes.diabetesjournals.org/cgi/doi/10.2337/diabetes.52.4.1031 PubMed PMID: 12663476. doi: 10.2337/diabetes.52.4.1031
20. Nakatsue T, Koike H, Han GD, Suzuki K, Miyauchi N, Yuan H, et al. Nephrin and podocin dissociate at the onset of proteinuria in experimental membranous nephropathy. Kidney Int 2005;67(6):2239-2253. Available from: http://www.nature.com/doifinder/10.1111/j.1523-1755.2005.00328.x PubMed PMID: 15882266. doi: 10.1111/j.1523-1755.2005.00328.x
21. Huh W. Expression of nephrin in acquired human glomerular disease. Nephrology Dialysis Transplantation 2002;17(3):478-484. Available from: http://ndt.oxfordjournals.org/cgi/doi/10.1093/ndt/17.3.478 PubMed PMID: 11865096. doi: 10.1093/ndt/17.3.478
22. Ng DPK, Tai BC, Tan E, Leong H, Nurbaya S, Lim XL, et al. Nephrinuria associates with multiple renal traits in type 2 diabetes. Nephrology Dialysis Transplantation 2011;26(8):2508-2514. Available from: http://ndt.oxfordjournals.org/cgi/doi/10.1093/ndt/gfq738 PubMed PMID: 21196468. doi: 10.1093/ndt/gfq738
23. Jim B, Ghanta M, Qipo A, Fan Y, Chuang PY, Cohen HW, et al. Dysregulated nephrin in diabetic nephropathy of type 2 diabetes: a cross sectional study. PLoS One 2012;7(5):36041. Available from: http://dx.plos.org/10.1371/journal.pone.0036041 PubMed PMID: 22615747. doi: 10.1371/journal.pone.0036041
24. Patari A, Forsblom C, Havana M, Taipale H, Groop PH, Holthofer H. Nephrinuria in Diabetic Nephropathy of Type 1 Diabetes. Diabetes 2003;52(12):2969-2974. Available from: http://diabetes.diabetesjournals.org/cgi/doi/10.2337/diabetes.52.12.2969 PubMed PMID: 14633858. doi: 10.2337/diabetes.52.12.2969
25. Koop K. Expression of Podocyte-Associated Molecules in Acquired Human Kidney Diseases. Journal of the American Society of Nephrology 2003;14(8):2063-2071. Available from: http://www.jasn.org/cgi/doi/10.1097/01.ASN.0000078803.53165.C9 PubMed PMID: 12874460. doi: 10.1097/01.ASN.0000078803.53165.C9
26. Benigni A, Gagliardini E, Tomasoni S, Abbate M, Ruggenenti P, Kalluri R, et al. Selective impairment of gene expression and assembly of nephrin in human diabetic nephropathy. Kidney Int 2004;65(6):2193-2200. Available from: http://www.nature.com/doifinder/10.1111/j.1523-1755.2004.00636.x PubMed PMID: 15149332. doi: 10.1111/j.1523-1755.2004.00636.x
27. Chen H, Chen C, Guh J, Chang J, Shin S, Lai Y. Altering expression of α3β1 integrin on podocytes of human and rats with diabetes. Life Sciences 2000;67(19):2345-2353. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0024320500008158 PubMed PMID: 11065181. doi: 10.1016/S0024-3205(00)00815-8
28. Regoli M, Bendayan M. Alterations in the expression of the a 3 b 1 integrin in certain membrane domains of the glomerular epithelial cells (podocytes) in diabetes mellitus. Diabetologia 1997;40(1):15-22. Available from: http://link.springer.com/10.1007/s001250050637 doi: 10.1007/s001250050637
29. Nakamura T. Urinary excretion of podocytes in patients with diabetic nephropathy. Nephrology Dialysis Transplantation 2000;15(9):1379-1383. Available from: http://ndt.oxfordjournals.org/cgi/doi/10.1093/ndt/15.9.1379 PubMed PMID: 10978394. doi: 10.1093/ndt/15.9.1379
30. Vogelmann SU, Nelson WJ, Myers BD, Lemley KV. Urinary excretion of viable podocytes in health and renal disease. Am J Physiol Renal Physiol 2003;285(1):40-48. Available from: http://ajprenal.physiology.org/cgi/pmidlookup?view=long&pmid=12631553 PubMed PMID: 12631553. doi: 10.1152/ajprenal.00404.2002
31. Sanchez-Niño MD, Sanz AB, Sanchez-Lopez E, Ruiz-Ortega M, Benito-Martin A, Saleem MA, et al. HSP27/HSPB1 as an adaptive podocyte antiapoptotic protein activated by high glucose and angiotensin II. Lab Invest 2012;92(1):32-45. Available from: http://www.nature.com/doifinder/10.1038/labinvest.2011.138 PubMed PMID: 21931298. doi: 10.1038/labinvest.2011.138
32. Susztak K. Glucose-Induced Reactive Oxygen Species Cause Apoptosis of Podocytes and Podocyte Depletion at the Onset of Diabetic Nephropathy. Diabetes 2006;55(1):225-233. Available from: http://diabetes.diabetesjournals.org/cgi/doi/10.2337/diabetes.55.01.06.db05-0894 PubMed PMID: 16380497. doi: 10.2337/diabetes.55.01.06.db05-0894
33. Verzola D, Gandolfo MT, Ferrario F, Rastaldi MP, Villaggio B, Gianiorio F, et al. Apoptosis in the kidneys of patients with type II diabetic nephropathy. Kidney Int 2007;72(10):1262-1272. Available from: http://www.nlm.nih.gov/medlineplus/diabetestype2.html PubMed PMID: 17851466. doi: 10.1038/sj.ki.5002531
34. Liu Y. New Insights into Epithelial-Mesenchymal Transition in Kidney Fibrosis. Journal of the American Society of Nephrology 2010;21(2):212-222. Available from: http://www.jasn.org/cgi/doi/10.1681/ASN.2008121226 doi: 10.1681/ASN.2008121226
35. Wolf G, Wenzel U, Ziyadeh FN, Stahl RAK. Angiotensin converting-enzyme inhibitor treatment reduces glomerular p16 INK4 and p27 Kip1 expression in diabetic BBdp rats. Diabetologia 1999;42(12):1425-1432. Available from: http://link.springer.com/10.1007/s001250051314 PubMed PMID: 10651261. doi: 10.1007/s001250051314
36. Griffin SV, Petermann AT, Durvasula RV, Shankland SJ. Podocyte proliferation and differentiation in glomerular disease: role of cell-cycle regulatory proteins. Nephrol Dial Transplant 2003;18(6):8-13. doi: 10.1093/ndt/gfg1069
37. Xu Z, Yoo T, Ryu D, Cheon Park H, Ha SK, Han DS, et al. Angiotensin II receptor blocker inhibits p27Kip1 expression in glucose-stimulated podocytes and in diabetic glomeruli. Kidney Int 2005;67(3):944-952. Available from: http://www.nature.com/doifinder/10.1111/j.1523-1755.2005.00158.x PubMed PMID: 15698433. doi: 10.1111/j.1523-1755.2005.00158.x
38. Hoshi S, Shu Y, Yoshida F, Inagaki T, Sonoda J, Watanabe T, et al. Podocyte Injury Promotes Progressive Nephropathy in Zucker Diabetic Fatty Rats. Lab Invest 2002;82(1):25-35. Available from: http://www.nature.com/doifinder/10.1038/labinvest.3780392 PubMed PMID: 11796823. doi: 10.1038/labinvest.3780392
39. Kriz W, LeHir M. Pathways to nephron loss starting from glomerular diseases-Insights from animal models. Kidney Int 2005;67(2):404-419. Available from: http://www.nature.com/doifinder/10.1111/j.1523-1755.2005.67097.x doi: 10.1111/j.1523-1755.2005.67097.x
40. Wiggins RC. The spectrum of podocytopathies: A unifying view of glomerular diseases. Kidney Int 2007;71(12):1205-1214. Available from: http://www.nature.com/doifinder/10.1038/sj.ki.5002222 PubMed PMID: 17410103. doi: 10.1038/sj.ki.5002222
41. Steffes MW, Schmidt D, Mccrery R, Basgen JM, Group IDN. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 2001;59(6):2104-2113. Available from: http://www.nature.com/doifinder/10.1046/j.1523-1755.2001.00725.x doi: 10.1046/j.1523-1755.2001.00725.x
42. Meyer TW, Bennett PH, Nelson RG. Podocyte number predicts long-term urinary albumin excretion in Pima Indians with Type II diabetes and microalbuminuria. Diabetologia 1999;42(11):1341-1344. Available from: http://www.diseaseinfosearch.org/result/2236 PubMed PMID: 10550418. doi: 10.1007/s001250051447
43. White KE, Bilous RW. Structural alterations to the podocyte are related to proteinuria in type 2 diabetic patients. Nephrology Dialysis Transplantation 2004;19(6):1437-1440. Available from: http://ndt.oxfordjournals.org/cgi/doi/10.1093/ndt/gfh129 PubMed PMID: 14993494. doi: 10.1093/ndt/gfh129
44. Abbate M, Zoja C, Morigi M, Rottoli D, Angioletti S, Tomasoni S, et al. Transforming Growth Factor-β1 Is Up-Regulated by Podocytes in Response to Excess Intraglomerular Passage of Proteins. The American Journal of Pathology 2002;161(6):2179-2193. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0002944010644951 PubMed PMID: 12466133. doi: 10.1016/S0002-9440(10)64495-1
45. Durvasula RV, Petermann AT, Hiromura K, Blonski M, Pippin J, Mundel P, et al. Activation of a local tissue angiotensin system in podocytes by mechanical strain1. Kidney Int 2004;65(1):30-39. Available from: http://www.nature.com/doifinder/10.1111/j.1523-1755.2004.00362.x PubMed PMID: 14675034. doi: 10.1111/j.1523-1755.2004.00362.x
46. Ichihara A, Kaneshiro Y, Takemitsu T, Sakoda M, Itoh H. The (pro)renin receptor and the kidney. Semin Nephrol 2007;27(5):524-528. Available from: http://ghr.nlm.nih.gov/gene=REN PubMed PMID: 17868789. doi: 10.1016/j.semnephrol.2007.07.005
47. Parving H, Persson F, Lewis JB, Lewis EJ, Hollenberg NK. Aliskiren Combined with Losartan in Type 2 Diabetes and Nephropathy. N Engl J Med 2008;358(23):2433-2446. Available from: http://www.nejm.org/doi/abs/10.1056/NEJMoa0708379 PubMed PMID: 18525041. doi: 10.1056/NEJMoa0708379
48. Ding G, Reddy K, Kapasi AA, Franki N, Gibbons N, Kasinath BS, et al. Angiotensin II induces apoptosis in rat glomerular epithelial cells. Am J Physiol Renal Physiol 2002;283(1):173-180. doi: 10.1152/ajprenal.00240.2001
49. Schiffer M, Mundel P, Shaw AS, Bottinger EP. A Novel Role for the Adaptor Molecule CD2-associated Protein in Transforming Growth Factor- -induced Apoptosis. Journal of Biological Chemistry 2004;279(35):37004-37012. Available from: http://www.jbc.org/cgi/doi/10.1074/jbc.M403534200 PubMed PMID: 15213232. doi: 10.1074/jbc.M403534200
50. Gilbert RE, Mifsud SA, Hulthen UL, Wilkinson-Berka JL, Bertram JF, Allen TJ, et al. Podocyte foot process broadening in experimental diabetic nephropathy: amelioration with renin-angiotensin blockade. Diabetologia 2001;44(7):878-882. Available from: http://link.springer.com/10.1007/s001250100561 PubMed PMID: 11508273. doi: 10.1007/s001250100561
51. Gross ML, El-Shakmak A, Szábó A, Koch A, Kuhlmann A, Münter K. ACE-inhibitors but not endothelin receptor blockers prevent podocyte loss in early diabetic nephropathy. Diabetologia 2003;46(6):856-868. Available from: http://link.springer.com/10.1007/s00125-003-1106-8 doi: 10.1007/s00125-003-1106-8
52. Flannery PJ, Spurney RF. Transactivation of epidermal growth factor receptor by angiotensin II in glomerular podocytes. Nephron Exp Nephrol. 2006;103(3):e109-118. doi:10.1159/000092196
53. Yard BA, Kahlert S, Engelleiter R, Resch S, Waldherr R, Groffen AJ, et al. Decreased Glomerular Expression of Agrin in Diabetic Nephropathy and Podocytes, Cultured in High Glucose Medium. Nephron Experimental Nephrology 2001;9(3):214-222. Available from: http://www.karger.com/doi/10.1159/000052614 doi: 10.1159/000052614
54. Chen S, Lee JS, Iglesias-de la Cruz, M C , Wang A, Izquierdo-Lahuerta A, Gandhi NK, et al. Angiotensin II stimulates 3(IV) collagen production in mouse podocytes via TGF- and VEGF signalling: implications for diabetic glomerulopathy. Nephrology Dialysis Transplantation 2005;20(7):1320-1328. Available from: http://ndt.oxfordjournals.org/cgi/doi/10.1093/ndt/gfh837 PubMed PMID: 15840669. doi: 10.1093/ndt/gfh837
55. Wolf G. Free radical production and angiotensin. Current Science Inc 2000;2(2):167-173. Available from: http://link.springer.com/10.1007/s11906-000-0078-z PubMed PMID: 10981145. doi: 10.1007/s11906-000-0078-z
56. Kriz W, LeHir M. Pathways to nephron loss starting from glomerular diseases-Insights from animal models. Kidney Int 2005;67(2):404-419. Available from: http://www.nature.com/doifinder/10.1111/j.1523-1755.2005.67097.x PubMed PMID: 15673288. doi: 10.1111/j.1523-1755.2005.67097.x
57. Böttinger EP. TGF-β in Renal Injury and Disease. Seminars in Nephrology 2007;27(3):309-320. Available from: http://linkinghub.elsevier.com/retrieve/pii/S027092950700040X PubMed PMID: 17533008. doi: 10.1016/j.semnephrol.2007.02.009
58. Chen S, Jim B, Ziyadeh FN. Diabetic nephropathy and transforming growth factor-β: transforming our view of glomerulosclerosis and fibrosis build-up. Seminars in Nephrology 2003;23(6):532-543. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0270929503001323 doi: 10.1053/S0270-9295(03)00132-3
59. Leask A, Abraham DJ. TGF- signaling and the fibrotic response. The FASEB Journal 2004;18(7):816-827. Available from: http://www.fasebj.org/cgi/doi/10.1096/fj.03-1273rev PubMed PMID: 15117886. doi: 10.1096/fj.03-1273rev
60. Li Y, Kang YS, Dai C, Kiss LP, Wen X, Liu Y. Epithelial-to-Mesenchymal Transition Is a Potential Pathway Leading to Podocyte Dysfunction and Proteinuria. The American Journal of Pathology 2008;172(2):299-308. Available from: http://linkinghub.elsevier.com/retrieve/pii/S000294401061797X PubMed PMID: 18202193. doi: 10.2353/ajpath.2008.070057
61. Yamaguchi Y, Iwano M, Suzuki D, Nakatani K, Kimura K, Harada K, et al. Epithelial-Mesenchymal Transition as a Potential Explanation for Podocyte Depletion in Diabetic Nephropathy. American Journal of Kidney Diseases 2009;54(4):653-664. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0272638609008324 PubMed PMID: 19615802. doi: 10.1053/j.ajkd.2009.05.009
62. Tufro A, Veron D. VEGF and Podocytes in Diabetic Nephropathy. Seminars in Nephrology 2012;32(4):385-393. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0270929512000885 doi: 10.1016/j.semnephrol.2012.06.010
63. Veron D, Bertuccio CA, Marlier A, Reidy K, Garcia AM, Jimenez J, et al. Podocyte vascular endothelial growth factor (Vegf 164 ) overexpression causes severe nodular glomerulosclerosis in a mouse model of type 1 diabetes. Diabetologia 2011;54(5):1227-1241. Available from: http://link.springer.com/10.1007/s00125-010-2034-z doi: 10.1007/s00125-010-2034-z
64. Kim NH, Kim KB, Kim DL, Kim SG, Choi KM, Baik SH, et al. Plasma and urinary vascular endothelial growth factor and diabetic nephropathy in Type 2 diabetes mellitus. Diabet Med 2004;21(6):545-551. Available from: http://doi.wiley.com/10.1111/j.1464-5491.2004.01200.x PubMed PMID: 15154937. doi: 10.1111/j.1464-5491.2004.01200.x
65. Fan Q, Xing Y, Ding J, Guan N. Reduction in VEGF protein and phosphorylated nephrin associated with proteinuria in adriamycin nephropathy rats. Nephron Exp Nephrol 2009;111(4):10-1159. Available from: http://toxnet.nlm.nih.gov/cgi-bin/sis/search/r?dbs+hsdb:@term+@rn+23214-92-8 PubMed PMID: 19293598. doi: 10.1159/000209209
66. Foster RR, Saleem MA, Mathieson PW, Bates DO, Harper SJ. Vascular endothelial growth factor and nephrin interact and reduce apoptosis in human podocytes. Am J Physiol Renal Physiol 2004;288(1):48-57. Available from: http://ajprenal.physiology.org/cgi/pmidlookup?view=long&pmid=15339792 PubMed PMID: 15339792. doi: 10.1152/ajprenal.00146.2004
67. Nakamura T, Ushiyama C, Osada S, Hara M, Shimada N, Koide H. Pioglitazone reduces urinary podocyte excretion in type 2 diabetes patients with microalbuminuria. Metabolism 2001;50(10):1193-1196. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0026049501320231 PubMed PMID: 11586492. doi: 10.1053/meta.2001.26703
68. Zhang Y, Guan Y. PPAR-γ agonists and diabetic nephropathy. Curr Diab Rep 2005;5(6):470-475. Available from: http://link.springer.com/10.1007/s11892-005-0057-5 PubMed PMID: 16316600. doi: 10.1007/s11892-005-0057-5
69. Benigni A. Transcriptional Regulation of Nephrin Gene by Peroxisome Proliferator-Activated Receptor- Agonist: Molecular Mechanism of the Antiproteinuric Effect of Pioglitazone. Journal of the American Society of Nephrology 2006;17(6):1624-1632. Available from: http://www.jasn.org/cgi/doi/10.1681/ASN.2005090983 PubMed PMID: 16687628. doi: 10.1681/ASN.2005090983
70. Lennon R, Welsh GI, Singh A, Satchell SC, Coward RJ, Tavaré JM, et al. Rosiglitazone enhances glucose uptake in glomerular podocytes using the glucose transporter GLUT1. Diabetologia 2009;52(9):1944-1952. Available from: http://link.springer.com/10.1007/s00125-009-1423-7 PubMed PMID: 19533082. doi: 10.1007/s00125-009-1423-7
71. Zhang H, Saha J, Byun J, Schin M, Lorenz M, Kennedy RT, et al. Rosiglitazone reduces renal and plasma markers of oxidative injury and reverses urinary metabolite abnormalities in the amelioration of diabetic nephropathy. Am J Physiol Renal Physiol 2008;295(4):1071-1081. Available from: http://ajprenal.physiology.org/cgi/pmidlookup?view=long&pmid=18667486 PubMed PMID: 18667486. doi: 10.1152/ajprenal.90208.2008
72. Kryachkova AA, Savelyeva SA, Gallyamov MG, Shestakova MV, Kutyrina IM. The role of obesity in renal injury in patients with metabolic syndrome. Nefrologii︠a︡ i dializ 2010;12(1):34-38.
73. Савельева СА, Крячкова АА, Курумова КО, Шамхалова МШ, Кутырина ИМ, Шестакова МВ. Ожирение – фактор риска поражения почек у больных сахарным диабетом 2 типа. Сахарный диабет. 2010; (2): 45-49. [Savel'eva SA, Kryachkova AA, Kurumova KO, Shamkhalova MS, Kutyrina IM, Shestakova MV. Obesity - a risk factor of renal pathology in patients with type 2 diabetes mellitus. Diabetes mellitus. 2010;(2):45-49.] doi: 10.14341/2072-0351-5673
74. Сагинова ЕА, Северова ММ, Галлямов МГ, Ермаков НВ, Родина АВ, Фомин ВВ, и др. Клиническое значение адипонектинемии в формировании поражения органов-мишеней при метаболическом синдроме, ассоциированном с неалкогольной жировой болезнью печени. Клиническая нефрология. 2011;(6):36-41. [Saginova EA, Severova MM, Gallyamov MG, Ermakov NV, Rodina AV, Fomin VV, i dr. Klinicheskoe znachenie adiponektinemii v formirovanii porazheniya organov-misheney pri metabolicheskom sindrome, assotsiirovannom s nealkogol'noy zhirovoy bolezn'yu pecheni. Klinicheskai︠a︡ nefrologii︠a︡. 2011;(6):36-41.]
75. Sharma K, Ramachandrarao S, Qiu G, Usui HK, Zhu Y, Dunn SR, et al. Adiponectin regulates albuminuria and podocyte function in mice. J Clin Invest. 2008;118(5):1645-1656. doi: 10.1172/JCI32691
76. Lee MH, Song HK, Ko GJ, Kang YS, Han SY, Han KH, et al. Angiotensin receptor blockers improve insulin resistance in type 2 diabetic rats by modulating adipose tissue. Kidney Int. 2008;74(7):890-900. doi: 10.1038/ki.2008.313
77. Lenz O, Fornoni A. Renin-angiotensin system blockade and diabetes: moving the adipose organ from the periphery to the center. Kidney Int. 2008;74(7):851-853. doi: 10.1038/ki.2008.391
78. Harvey SJ, Jarad G, Cunningham J, Goldberg S, Schermer B, Harfe BD, et al. Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol. 2008;19(11):2150-2158. doi: 10.1681/ASN.2008020233
79. Ho J, Ng KH, Rosen S, Dostal A, Gregory RI, Kreidberg JA. Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J Am Soc Nephrol. 2008;19(11):2069-2075. doi: 10.1681/ASN.2008020162
80. Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, et al. MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A. 2007;104(9):3432-3437. doi: 10.1073/pnas.0611192104
Review
For citations:
Bobkova I.N., Shestakova M.V., Shchukina A.A. Podocyte injury in diabetes mellitus. Diabetes mellitus. 2014;17(3):39-50. (In Russ.)
Views:
2267
Email this article 
