Podocyte-specific overexpression of the antioxidant metallothionein reduces diabetic nephropathy

Journal of the American Society of Nephrology

Volumn 19, Issue 11, 2008, Pages 2077-2085

  Zheng, Shirong ^a   Carlson, Edward C ^b   Yang, Lu ^a   Kralik, Patricia M ^a   Huang, Yun ^a   Epstein, Paul N ^a  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; METALLOTHIONEIN; ANTIOXIDANT; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL DAMAGE; CELL FUNCTION; CELL PROTECTION; CELL SPECIFICITY; CELL STRUCTURE; CELL VOLUME; CONTROLLED STUDY; CROSS BREEDING; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISEASE COURSE; GENE OVEREXPRESSION; GLOMERULUS; KIDNEY; MALE; MESANGIUM CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PODOCYTE; PRIORITY JOURNAL; RENAL PROTECTION; STRAIN DIFFERENCE; TRANSGENE; TRANSGENIC MOUSE; URINARY EXCRETION; ALBUMINURIA; ANIMAL; APOPTOSIS; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; PATHOLOGY;

ALBUMINURIA; ANIMALS; ANTIOXIDANTS; APOPTOSIS; DIABETIC NEPHROPATHIES; GENE EXPRESSION; HUMANS; KIDNEY GLOMERULUS; METALLOTHIONEIN; MICE; MICE, TRANSGENIC; OXIDATIVE STRESS; PODOCYTES; RECOMBINANT PROTEINS;

EID: 55749110018     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2007080967     Document Type: Article

References (42)

1. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 329: 977-986, 1993
2. Abbott K, Basta E, Bakris GL: Blood pressure control and nephroprotection in diabetes. J Clin Pharmacol 44: 431-438, 2004
3. Gurley SB, Coffman TM: The renin-angiotensin system and diabetic nephropathy. Semin Nephrol 27: 144-152, 2007
4. Abbate M, Zoja C, Rottoli D, Corna D, Perico N, Bertani T, Remuzzi G: Antiproteinuric therapy while preventing the abnormal protein traffic in proximal tubule abrogates protein- and complement-dependent interstitial inflammation in experimental renal disease. J Am Soc Nephrol 10: 804-813, 1999
5. Abbate M, Zoja C, Remuzzi G: How does proteinuria cause progressive renal damage? J Am Soc Nephrol 17: 2974-2984, 2006
6. Kiritoshi S, Nishikawa T, Sonoda K, Kukidome D, Senokuchi T, Matsuo T, Matsumura T, Tokunaga H, Brownlee M, Araki E: Reactive oxygen species from mitochondria induce cyclooxygenase-2 gene expression in human mesangial cells: Potential role in diabetic nephropathy. Diabetes 52: 2570-2577, 2003
7. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M: Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790, 2000
8. Craven PA, Melhem MF, Phillips SL, DeRubertis FR: Overexpression of Cu2+/Zn2+ superoxide dismutase protects against early diabetic glomerular injury in transgenic mice. Diabetes 50: 2114-2125, 2001
9. DeRubertis FR, Craven PA, Melhem MF, Salah EM: Attenuation of renal injury in db/db mice overexpressing superoxide dismutase: Evidence for reduced superoxide-nitric oxide interaction. Diabetes 53: 762-768, 2004
10. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG, Coplon NS, Sun L, Meyer TW: Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99: 342-348, 1997
11. Steffes MW, Schmidt D, McCrery R, Basgen JM: Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 59: 2104-2113, 2001
12. Susztak K, Raff AC, Schiffer M, Bottinger EP: Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 55: 225-233, 2006
13. Binder CJ, Weiher H, Exner M, Kerjaschki D: Glomerular overproduction of oxygen radicals in Mpv17 gene-inactivated mice causes podocyte foot process flattening and proteinuria: A model of steroidresistant nephrosis sensitive to radical scavenger therapy. Am J Pathol 154: 1067-1075, 1999
14. Greiber S, Munzel T, Kastner S, Muller B, Schollmeyer P, Pavenstadt H: NAD(P)H oxidase activity in cultured human podocytes: Effects of adenosine triphosphate. Kidney Int 53: 654-663, 1998
15. Epstein PN, Overbeek PA, Means AR: Calmodulin-induced early-onset diabetes in transgenic mice. Cell 58: 1067-1073, 1989
16. Zheng S, Noonan WT, Metreveli NS, Coventry S, Kralik PM, Carlson EC, Epstein PN: Development of late-stage diabetic nephropathy in OVE26 diabetic mice. Diabetes 53: 3248-3257, 2004
17. Sanden SK, Wiggins JE, Goyal M, Riggs LK, Wiggins RC: Evaluation of a thick and thin section method for estimation of podocyte number, glomerular volume, and glomerular volume per podocyte in rat kidney with Wilms' tumor-1 protein used as a podocyte nuclear marker. J Am Soc Nephrol 14: 2484-2493, 2003
18. Basgen JM, Nicholas SB, Mauer M, Rozen S, Nyengaard JR: Comparison of methods for counting cells in the mouse glomerulus. Nephron Exp Nephrol 103: e139-e148, 2006
19. Vissers MC, Winterbourn CC: The effect of oxidants on neutrophil-mediated degradation of glomerular basement membrane collagen. Biochim Biophys Acta 889: 277-286, 1986
20. Shah SV: The role of reactive oxygen metabolites in glomerular disease. Annu Rev Physiol 57: 245-262, 1995
21. Suzuki D, Miyata T: Carbonyl stress in the pathogenesis of diabetic nephropathy. Intern Med 38: 309-314, 1999
22. Melhem MF, Craven PA, Liachenko J, DeRubertis FR: Alpha-lipoic acid attenuates hyperglycemia and prevents glomerular mesangial matrix expansion in diabetes. J Am Soc Nephrol 13: 108-116, 2002
23. Melhem MF, Craven PA, DeRubertis FR: Effects of dietary supplementation of alpha-lipoic acid on early glomerular injury in diabetes mellitus. J Am Soc Nephrol 12: 124-133, 2001
24. Koya D, Hayashi K, Kitada M, Kashiwagi A, Kikkawa R, Haneda M: Effects of antioxidants in diabetes-induced oxidative stress in the glomeruli of diabetic rats. J Am Soc Nephrol 14: S250-S253, 2003
25. Moeller MJ, Kovari IA, Holzman LB: Evaluation of a new tool for exploring podocyte biology: Mouse Nphs1 5′ flanking region drives LacZ expression in podocytes. J Am Soc Nephrol 11: 2306-2314, 2000
26. Kumari MV, Hiramatsu M, Ebadi M: Free radical scavenging actions of metallothionein isoforms I and II. Free Radic Res 29: 93-101, 1998
27. Miura T, Muraoka S, Ogiso T: Antioxidant activity of metallothionein compared with reduced glutathione. Life Sci 60: L-9, 1997
28. Li X, Chen H, Epstein PN: Metallothionein protects islets from hypoxia and extends islet graft survival by scavenging most kinds of reactive oxygen species. J Biol Chem 279: 765-771, 2004
29. Schwarz MA, Lazo JS, Yalowich JC, Allen WP, Whitmore M, Bergonia HA, Tzeng E, Billiar TR, Robbins PD, Lancaster JR Jr: Metallothionein protects against the cytotoxic and DNA-damaging effects of nitric oxide. Proc Natl Acad Sci U S A 92: 4452-4456, 1995
30. Liang Q, Carlson EC, Donthi RV, Kralik PM, Shen X, Epstein PN: Overexpression of metallothionein reduces diabetic cardiomyopathy. Diabetes 51: 174-181, 2002
31. Chen H, Carlson EC, Pellet L, Moritz JT, Epstein PN: Overexpression of metallothionein in pancreatic beta-cells reduces streptozotocin-induced DNA damage and diabetes. Diabetes 50: 2040-2046, 2001
32. Li X, Chen H, Epstein PN: Metallothionein and catalase sensitize to diabetes in nonobese diabetic mice: Reactive oxygen species may have a protective role in pancreatic beta-cells. Diabetes 55: 1592-1604, 2006
33. Palmiter RD, Brinster RL: Germ-line transformation of mice. Annu Rev Genet 20: 465-499, 1986
34. Toyoda M, Najafian B, Kim Y, Caramori ML, Mauer M: Podocyte detachment and reduced glomerular capillary endothelial fenestration in human type 1 diabetic nephropathy. Diabetes 56: 2155-2160, 2007
35. Pavenstadt H, Kriz W, Kretzler M: Cell biology of the glomerular podocyte. Physiol Rev 83: 253-307, 2003
36. Neale TJ, Ullrich R, Ojha P, Poczewski H, Verhoeven AJ, Kerjaschki D: Reactive oxygen species and neutrophil respiratory burst cytochrome b558 are produced by kidney glomerular cells in passive Heymann nephritis. Proc Natl Acad Sci U S A 90: 3645-3649, 1993
37. Wang D, Yang JY, Wang PL: The interaction of glomerular mesangial cells and epithelial cells. Pediatr Nephrol 12: 197-200, 1998
38. Wharram BL, Goyal M, Wiggins JE, Sanden SK, Hussain S, Filipiak WE, Saunders TL, Dysko RC, Kohno K, Holzman LB, Wiggins RC: Podocyte depletion causes glomerulosclerosis: Diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol 16: 2941-2952, 2005
39. Takemoto M, Asker N, Gerhardt H, Lundkvist A, Johansson BR, Saito Y, Betsholtz C: A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 161: 799-805, 2002
40. Kim YH, Goyal M, Kurnit D, Wharram B, Wiggins J, Holzman L, Kershaw D, Wiggins R: Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat. Kidney Int 60: 957-968, 2001
41. Weibel ER: Practical Methods for Biological Morphometry: Stereological Methods, London, London Academic Press, 1979
42. Mifsud SA, Allen TJ, Bertram JF, Hulthen UL, Kelly DJ, Cooper ME, Wilkinson-Berka JL, Gilbert RE: Podocyte foot process broadening in experimental diabetic nephropathy: Amelioration with renin-angiotensin blockade. Diabetologia 44: 878-882, 2001