Differences in susceptibility to develop parameters of diabetic nephropathy in four mouse strains with type 1 diabetes

American Journal of Physiology - Renal Physiology

Volumn 306, Issue 10, 2014, Pages

  Franzén, Stephanie ^a   Friederich Persson, Malou ^b   Fasching, Angelica ^b   Hansell, Peter ^b   Nangaku, Masaomi ^c   Palm, Fredrik ^a,b  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

129Sv; BALB c; C57Bl 6; Diabetic nephropathy; Kidney function; NMRI

Indexed keywords

ALLOXAN; CREATININE; POTASSIUM ION; SODIUM ION; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

129X1/SV MOUSE; ALLOXAN-INDUCED DIABETES MELLITUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CONTROLLED STUDY; CREATININE URINE LEVEL; DIABETIC NEPHROPATHY; DISEASE COURSE; DISEASE PREDISPOSITION; ELECTROLYTE URINE LEVEL; GLOMERULOPATHY; GLOMERULUS FILTRATION RATE; HISTOPATHOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; MOUSE STRAIN; NMRI MOUSE; NONHUMAN; OXIDATIVE STRESS; PERIODIC ACID SCHIFF STAIN; POTASSIUM EXCRETION; PRIORITY JOURNAL; PROTEINURIA; SODIUM EXCRETION; ULTRAFILTRATION;

129SV; BALB/C; C57BL/6; DIABETIC NEPHROPATHY; KIDNEY FUNCTION; NMRI;

ALLOXAN; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; GLOMERULAR FILTRATION RATE; INCIDENCE; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED STRAINS; OXIDATIVE STRESS; PROTEINURIA; RISK FACTORS; SPECIES SPECIFICITY;

EID: 84900818423     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00595.2013     Document Type: Article

References (65)

1. Allen TJ, Cooper ME, Lan HY. Use of genetic mouse models in the study of diabetic nephropathy. Curr Diab Rep 4: 435-440, 2004.
2. Alm AS, Li K, Yang D, Andersson R, Lu Y, Wang X. Varying susceptibility of pulmonary cytokine production to lipopolysaccharide in mice. Cytokine 49: 256-263, 2010.
3. Antvorskov JC, Fundova P, Buschard K, Funda DP. Dietary gluten alters the balance of proinflammatory and anti-inflammatory cytokines in T cells of BALB/c mice. Immunology 138: 23-33, 2012.
4. Apakkan Aksun S, Ozmen B, Ozmen D, Parildar Z, Senol B, Habif S, Mutaf I, Turgan N, Bayindir O. Serum and urinary nitric oxide in Type 2 diabetes with or without microalbuminuria: relation to glomerular hyperfiltration. J Diabetes Complications 17: 343-348, 2003.
5. Dachs S, Churg J, Mautner W, Grishman E. Diabeticnephropathy. Am J Pathol 44: 155-168, 1964.
6. de Jong PE, Gansevoort RT. Albuminuria in non-primary renal disease: risk marker rather than risk factor. Nephrol Dial Transplant 25: 656-658, 2010.
7. Deerberg F, Gleichmann H. The occurrence of spontaneous immunecomplex glomerulonephritis in Han: NMRI mice. Contrib Nephrol 19: 88-94, 1980.
8. Dugan LL, You YH, Ali SS, Diamond-Stanic M, Miyamoto S, De-Cleves AE, Andreyev A, Quach T, Ly S, Shekhtman G, Nguyen W, Chepetan A, Le TP, Wang L, Xu M, Paik KP, Fogo A, Viollet B, Murphy A, Brosius F, Naviaux RK, Sharma K. AMPK dysregulation promotes diabetes-related reduction of superoxide and mitochondrial function. J Clin Invest 123: 4888-4899, 2013.
9. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD. Superoxide activates mitochondrial uncoupling proteins. Nature 415: 96-99, 2002.
10. Faulhaber-Walter R, Chen L, Oppermann M, Kim SM, Huang Y, Hiramatsu N, Mizel D, Kajiyama H, Zerfas P, Briggs JP, Kopp JB, Schnermann J. Lack of A1 adenosine receptors augments diabetic hyperfiltration and glomerular injury. J Am Soc Nephrol 19: 722-730, 2008.
11. Ficociello LH, Perkins BA, Roshan B, Weinberg JM, Aschengrau A, Warram JH, Krolewski AS. Renal hyperfiltration and the development of microalbuminuria in type 1 diabetes. Diabetes Care 32: 889-893, 2009.
12. Fioretto P, Caramori ML, Mauer M. The kidney in diabetes: dynamic pathways of injury and repair. The Camillo Golgi Lecture 2007. Diabetologia 51: 1347-1355, 2008.
13. Friederich M, Fasching A, Hansell P, Nordquist L, Palm F. Diabetesinduced up-regulation of uncoupling protein-2 results in increased mitochondrial uncoupling in kidney proximal tubular cells. Biochim Biophys Acta 1777: 935-940, 2008.
14. Gross ML, El-Shakmak A, Szabo A, Koch A, Kuhlmann A, Munter K, Ritz E, Amann K. ACE-inhibitors but not endothelin receptor blockers prevent podocyte loss in early diabetic nephropathy. Diabetologia 46: 856-868, 2003.
15. Gurley SB, Clare SE, Snow KP, Hu A, Meyer TW, Coffman TM. Impact of genetic background on nephropathy in diabetic mice. Am J Physiol Renal Physiol 290: F214-F222, 2006.
16. Hong SW, Isono M, Chen S, Iglesias-De La Cruz MC, Han DC, Ziyadeh FN. Increased glomerular and tubular expression of transforming growth factor-beta1, its type II receptor, and activation of the Smad signaling pathway in the db/db mouse. Am J Pathol 158: 1653-1663, 2001.
17. Hovind P, Tarnow L, Rossing P, Jensen BR, Graae M, Torp I, Binder C, Parving HH. Predictors for the development of microalbuminuria and macroalbuminuria in patients with type 1 diabetes: inception cohort study. BMJ 328: 1105, 2004.
18. Inoue T, Kozawa E, Okada H, Inukai K, Watanabe S, Kikuta T, Watanabe Y, Takenaka T, Katayama S, Tanaka J, Suzuki H. Noninvasive evaluation of kidney hypoxia and fibrosis using magnetic resonance imaging. J Am Soc Nephrol 22: 1429-1434, 2011.
19. Jeansson M, Granqvist AB, Nyström JS, Haraldsson B. Functional and molecular alterations of the glomerular barrier in long-term diabetes in mice. Diabetologia 49: 2200-2209, 2006.
20. Jensen LJ, Denner L, Schrijvers BF, Tilton RG, Rasch R, Flyvbjerg A. Renal effects of a neutralising RAGE-antibody in long-term streptozotocin-diabetic mice. J Endocrinol 188: 493-501, 2006.
21. Jerums G, Premaratne E, Panagiotopoulos S, MacIsaac RJ. The clinical significance of hyperfiltration in diabetes. Diabetologia 53: 2093-2104, 2010.
22. Kulkarni RN, Almind K, Goren HJ, Winnay JN, Ueki K, Okada T, Kahn CR. Impact of genetic background on development of hyperinsulinemia and diabetes in insulin receptor/insulin receptor substrate-1 double heterozygous mice. Diabetes 52: 1528-1534, 2003.
23. Leyssac PP, Karlsen FM, Skøtt O. Role of proximal tubular reabsorption for the intrarenal control of GFR. Kidney Int Suppl 32: S132-135, 1991.
24. Magee GM, Bilous RW, Cardwell CR, Hunter SJ, Kee F, Fogarty DG. Is hyperfiltration associated with the future risk of developing diabetic nephropathy? A meta-analysis. Diabetologia 52: 691-697, 2009.
25. Matsubara T, Abe H, Arai H, Nagai K, Mima A, Kanamori H, Sumi E, Takahashi T, Matsuura M, Iehara N, Fukatsu A, Kita T, Doi T. Expression of Smad1 is directly associated with mesangial matrix expansion in rat diabetic nephropathy. Lab Invest 86: 357-368, 2006.
26. Mimura I, Nangaku M. The suffocating kidney: tubulointerstitial hypoxia in end-stage renal disease. Nat Rev Nephrol 6: 667-678, 2010.
27. Molitch ME, DeFronzo RA, Franz MJ, Keane WF, Mogensen CE, Parving HH, Steffes MW; American Diabetes Association. Nephropathy in diabetes. Diabetes Care 27, Suppl 1: S79-83, 2004.
28. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 17: 17-25, 2006.
29. Nangaku M. Hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. Nephron Exp Nephrol 98: e8-12, 2004.
30. 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.
31. Nishino T, Sasaki N, Nagasaki K, Ahmad Z, Agui T. Genetic background strongly influences the severity of glomerulosclerosis in mice. J Vet Med Sci 72: 1313-1318, 2010.
32. Nordquist L, Liss P, Fasching A, Hansell P, Palm F. Hypoxia in the diabetic kidney is independent of advanced glycation end-products. Adv Exp Med Biol 765: 185-193, 2013.
33. Ogawa S, Mori T, Nako K, Kato T, Takeuchi K, Ito S. Angiotensin II type 1 receptor blockers reduce urinary oxidative stress markers in hypertensive diabetic nephropathy. Hypertension 47: 699-705, 2006.
34. Palm F. Intrarenal oxygen in diabetes and a possible link to diabetic nephropathy. Clin Exp Pharmacol Physiol 33: 997-1001, 2006.
35. Palm F, Cederberg J, Hansell P, Liss P, Carlsson PO. Reactive oxygen species cause diabetes-induced decrease in renal oxygen tension. Diabetologia 46: 1153-1160, 2003.
36. Palm F, Friederich M, Carlsson PO, Hansell P, Teerlink T, Liss P. Reduced nitric oxide in diabetic kidneys due to increased hepatic arginine metabolism: implications for renomedullary oxygen availability. Am J Physiol Renal Physiol 294: F30-F37, 2008.
37. Palm F, Nangaku M, Fasching A, Tanaka T, Nordquist L, Hansell P, Kawakami T, Nishijima F, Fujita T. Uremia induces abnormal oxygen consumption in tubules and aggravates chronic hypoxia of the kidney via oxidative stress. Am J Physiol Renal Physiol 299: F380-F386, 2010.
38. Palm F, Nordquist L, Wilcox CS, Hansell P. Oxidative stress and hypoxia in the pathogenesis of diabetic nephropathy. In: Studies on Renal Disorders, edited by Miyata T, Eckardt KU, Nangaku M. New York: Humana, 2011, p. 559-586.
39. Persson MF, Franzen S, Catrina SB, Dallner G, Hansell P, Brismar K, Palm F. Coenzyme Q10 prevents GDP-sensitive mitochondrial uncoupling, glomerular hyperfiltration and proteinuria in kidneys from db/db mice as a model of type 2 diabetes. Diabetologia 55: 1535-1543, 2012.
40. Persson MF, Welch WJ, Wilcox CS, Palm F. Kidney function after in vivo gene silencing of uncoupling protein-2 in streptozotocin-induced diabetic rats. Adv Exp Med Biol 765: 217-223, 2013.
41. Persson P, Hansell P, Palm F. Adenosine A2 receptor-mediated regulation of renal hemodynamics and glomerular filtration rate is abolished in diabetes. Adv Exp Med Biol 765: 225-230, 2013.
42. Persson P, Hansell P, Palm F. Tubular reabsorption and diabetes-induced glomerular hyperfiltration. Acta Physiol (Oxf) 200: 3-10, 2010.
43. Prabhakar S, Starnes J, Shi S, Lonis B, Tran R. Diabetic nephropathy is associated with oxidative stress and decreased renal nitric oxide production. J Am Soc Nephrol 18: 2945-2952, 2007.
44. Ptak W, Hanczakowska M, Rozycka R, Rozycka D. Impaired antibody responses in alloxan diabetic mice. Clin Exp Immunol 29: 140-146, 1977.
45. Qi Z, Breyer MD. Measurement of glomerular filtration rate in conscious mice. Methods Mol Biol 466: 61-72, 2009.
46. Qi Z, Fujita H, Jin J, Davis LS, Wang Y, Fogo AB, Breyer MD. Characterization of susceptibility of inbred mouse strains to diabetic nephropathy. Diabetes 54: 2628-2637, 2005.
47. Qi Z, Whitt I, Mehta A, Jin J, Zhao M, Harris RC, Fogo AB, Breyer MD. Serial determination of glomerular filtration rate in conscious mice using FITC-inulin clearance. Am J Physiol Renal Physiol 286: F590-F596, 2004.
48. Ries M, Basseau F, Tyndal B, Jones R, Deminiere C, Catargi B, Combe C, Moonen CW, Grenier N. Renal diffusion and BOLD MRI in experimental diabetic nephropathy. Blood oxygen level-dependent. J Magn Reson Imaging 17: 104-113, 2003.
49. Rosenberger C, Khamaisi M, Abassi Z, Shilo V, Weksler-Zangen S, Goldfarb M, Shina A, Zibertrest F, Eckardt KU, Rosen S, Heyman SN. Adaptation to hypoxia in the diabetic rat kidney. Kidney Int 73: 34-42, 2008.
50. Rouschop KM, Sewnath ME, Claessen N, Roelofs JJ, Hoedemaeker I, van der Neut R, Aten J, Pals ST, Weening JJ, Florquin S. CD44 deficiency increases tubular damage but reduces renal fibrosis in obstructive nephropathy. J Am Soc Nephrol 15: 674-686, 2004.
51. Ruggenenti P, Perna A, Mosconi L, Pisoni R, Remuzzi G. Urinary protein excretion rate is the best independent predictor of ESRF in non-diabetic proteinuric chronic nephropathies. "Gruppo Italiano di Studi Epidemiologici in Nefrologia" (GISEN). Kidney Int 53: 1209-1216, 1998.
52. Sällström J, Carlsson PO, Fredholm BB, Larsson E, Persson AE, Palm F. Diabetes-induced hyperfiltration in adenosine A(1)-receptor deficient mice lacking the tubuloglomerular feedback mechanism. Acta Physiol (Oxf) 190: 253-259, 2007.
53. Scherzer P, Nachliel I, Bar-On H, Popovtzer MM, Ziv E. Renal Na-K-ATPase hyperactivity in diabetic Psammomys obesus is related to glomerular hyperfiltration but is insulin-independent. J Endocrinol 167: 347-354, 2000.
54. Stevens LA, Coresh J, Greene T, Levey AS. Assessing kidney function-measured and estimated glomerular filtration rate. N Engl J Med 354: 2473-2483, 2006.
55. Sugimoto H, Grahovac G, Zeisberg M, Kalluri R. Renal fibrosis and glomerulosclerosis in a new mouse model of diabetic nephropathy and its regression by bone morphogenic protein-7 and advanced glycation end product inhibitors. Diabetes 56: 1825-1833, 2007.
56. Suzuki D, Miyata T, Saotome N, Horie K, Inagi R, Yasuda Y, Uchida K, Izuhara Y, Yagame M, Sakai H, Kurokawa K. Immunohistochemical evidence for an increased oxidative stress and carbonyl modification of proteins in diabetic glomerular lesions. J Am Soc Nephrol 10: 822-832, 1999.
57. Teiken JM, Audettey JL, Laturnus DI, Zheng S, Epstein PN, Carlson EC. Podocyte loss in aging OVE26 diabetic mice. Anat Rec (Hoboken) 291: 114-121, 2008.
58. Thomas MC, Moran JL, Harjutsalo V, Thorn L, Waden J, Saraheimo M, Tolonen N, Leiviska J, Jula A, Forsblom C, Groop PH, Finn Diane Study Group. Hyperfiltration in type 1 diabetes: does it exist and does it matter for nephropathy? Diabetologia 55: 1505-1513, 2012.
59. Thomson SC, Vallon V, Blantz RC. Kidney function in early diabetes: the tubular hypothesis of glomerular filtration. Am J Physiol Renal Physiol 286: F8-F15, 2004.
60. Tojo A, Asaba K, Onozato ML. Suppressing renal NADPH oxidase to treat diabetic nephropathy. Expert Opin Ther Targets 11: 1011-1018, 2007.
61. Turin TC, James M, Ravani P, Tonelli M, Manns BJ, Quinn R, Jun M, Klarenbach S, Hemmelgarn BR. Proteinuria and rate of change in kidney function in a community-based population. J Am Soc Nephrol 24: 1661-1667, 2013.
62. Wajchenberg BL, Sabbaga E, Fonseca JA. The natural history of diabetic nephropathy in type I diabetes and the role of metabolic control in its prevention, reversibility and clinical course. Acta Diabetol Lat 20: 1-18, 1983.
63. Wilcox CS, Gutterman D. Focus on oxidative stress in the cardiovascular and renal systems. Am J Physiol Heart Circ Physiol 288: H3-H6, 2005.
64. Wirta O, Pasternack A, Mustonen J, Oksa H, Koivula T, Helin H. Albumin excretion rate and its relation to kidney disease in non-insulindependent diabetes mellitus. J Intern Med 237: 367-373, 1995.
65. Vucic Lovrencic M, Radisic Biljak V, Bozicevic S, Prasek M, Pavkovic P, Knotek M. Estimating glomerular filtration rate (GFR) in diabetes: the performance of MDRD and CKD-EPI equations in patients with various degrees of albuminuria. Clin Biochem 45: 1694-1696, 2012.