Nephron-deficient Fvb mice develop rapidly progressive renal failure and heavy albuminuria involving excess glomerular GLUT1 and VEGF

Laboratory Investigation

Volumn 90, Issue 1, 2010, Pages 83-97

  Wang, Youli ^a   Heilig, Kathleen O ^a,b   Minto, Andrew W ^a   Chen, Shenglin ^b   Xiang, Minghui ^b   Dean, David A ^c   Geiger, Richard C ^c   Chang, Anthony ^a   Pravtcheva, Dimitrina D ^d   Schlimme, Martin ^a   Deb, Dilip K ^a   Wang, Ying ^a   Heilig, Charles W ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d Department of Human Genetics   (United States)

Author keywords

FVB mouse; Glucose transporter; GLUT1; Oligosyndactyly; Renal failure; VEGF

Indexed keywords

ALBUMIN; FIBRONECTIN; GLUCOSE; GLUCOSE TRANSPORTER 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P50; SCLEROPROTEIN; VASCULOTROPIN;

ALBUMINURIA; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DISEASE COURSE; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; GLOMERULOSCLEROSIS; GLOMERULUS; GLUCOSE TRANSPORT; KIDNEY FAILURE; KIDNEY FUNCTION; KIDNEY HYPERTROPHY; KNOCKOUT MOUSE; MESANGIUM CELL; MOUSE; NEPHRON; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RENOVASCULAR HYPERTENSION; SIGNAL TRANSDUCTION; ULTRAFILTRATION; UPREGULATION; URINARY EXCRETION;

ALBUMINURIA; ALLELES; ANIMALS; CELLS, CULTURED; CREATININE; DISEASE PROGRESSION; EXTRACELLULAR MATRIX PROTEINS; GLOMERULAR MESANGIUM; GLUCOSE TRANSPORTER TYPE 1; IMMUNOHISTOCHEMISTRY; ISOENZYMES; KIDNEY; KIDNEY FAILURE; KIDNEY GLOMERULUS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROSCOPY, ELECTRON; NEPHRONS; NF-KAPPA B; PROTEIN KINASE C; STRESS, MECHANICAL; SYNDACTYLY; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 73349131400     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.95     Document Type: Article

References (60)

1. Brenner BM, Lawler EV, Mackenzie HS. The hyperfiltration theory: a paradigm shift in nephrology. Kidney Int 1996;49:1774-1777.
2. Drukker A. Oligonephropathy: from a rare childhood disorder to a possible health problem in the adult. Isr Med Assoc J 2002;4:191-195.
3. Brenner BM, Mackenzie HS. Nephron mass as a risk factor for progression of renal disease. Kidney Int Suppl 1997;63:S124-S127.
4. Brenner BM, Garcia DL, Anderson S. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens 1988;1:335-347.
5. Luyckx VA, Brenner BM. Low birth weight, nephron number, and kidney disease. Kidney Int Suppl 2005;97:S68-S77.
6. Woods LL. Neonatal uninephrectomy causes hypertension in adult rats. Am J Physiol 1999;276:R974-R978.
7. Moritz KM, Wintour EM, Dodic M. Fetal uninephrectomy leads to postnatal hypertension and compromised renal function. Hypertension 2002;39:1071-1076.
8. Mei-Zahav M, Korzets Z, Cohen I, et al. Ambulatory blood pressure monitoring in children with a solitary kidney\-a comparison between unilateral renal agenesis and uninephrectomy. Blood Press Monit 2001;6:263-267.
9. Brenner BM, Milford EL. Nephron underdosing: a programmed cause of chronic renal allograft failure. Am J Kidney Dis 1993;21:66-72.
10. Suzuki H, Tokuriki T, Kamita H, et al. Age-related pathophysiological changes in rat oligomeganephronic hypoplastic kidney. Pediatr Nephrol 2006;21:637-642.
11. Zalups RK. The Os/+ mouse: a genetic animal model of reduced renal mass. Am J Physiol 1993;264:F53-F60.
12. He C, Zalups RK, Henderson DA, et al. Molecular analysis of spontaneous glomerulosclerosis in Os/+ mice, a model with reduced nephron mass. Am J Physiol 1995;269:F266-F273.
13. He C, Esposito C, Phillips C, et al. Dissociation of glomerular hypertrophy, cell proliferation, and glomerulosclerosis in mouse strains heterozygous for a mutation (Os) which induces a 50% reduction in nephron number. J Clin Invest 1996;97:1242-1249.
14. Wise TL, Pravtcheva DD. Oligosyndactylism mice have an inversion of chromosome 8. Genetics 2004;168:2099-2112.
15. Pravtcheva DD, Wise TL. Disruption of Apc10/Doc1 in three alleles of oligosyndactylism. Genomics 2001;72:78-87.
16. Gruneberg H. Genetical studies on the skeleton of the mouse. XXVII. The development of oligosyndactylism. Genet Res Camb 1961;2:33-42.
17. Gruneberg H. Genetical studies on the skeleton of the mouse. XVIII. Three genes for syndactylism. Genetics 1956;54:113-145.
18. Lenz O, Zheng F, Vilar J, et al. The inheritance of glomerulosclerosis in mice is controlled by multiple quantitative trait loci. Nephrol Dial Transplant 1998;13:3074-3078.
19. Esposito C, He CJ, Striker GE, et al. Nature and severity of the glomerular response to nephron reduction is strain-dependent in mice. Am J Pathol 1999;154:891-897.
20. Oppermann M, Faulhaber-Walter R, Castrop H, et al. Glomerular hypertension and hyperfiltration in young fvb.ROP Os/+ mice. FASEB J 2007;21:595.28 (abstract).
21. Jarad G, Lakhe-Reddy S, Blatnik J, et al. Renal phenotype is exacerbated in Os and lpr double mutant mice. Kidney Int 2004;66:1029-1035.
22. Heilig CW, Concepcion LA, Riser BL, et al. Overexpression of glucose transporters in rat mesangial cells cultured in a normal glucose milieu mimics the diabetic phenotype. J Clin Invest 1995;96:1802-1814.
23. Heilig CW, Brosius III FC, Cunningham C. Role for GLUT1 in diabetic glomerulosclerosis. Expert Rev Mol Med 2006;8:1-18.
24. Gnudi L, Viberti G, Raij L, et al. GLUT-1 overexpression: link between hemodynamic and metabolic factors in glomerular injury? Hypertension 2003;42:19-24.
25. Heilig CW, Kreisberg JI, Freytag S, et al. Antisense GLUT-1 protects mesangial cells from glucose induction of GLUT-1 and fibronectin expression. Am J Physiol Renal Physiol 2001;280:F657-F666.
26. Heilig CW, Liu Y, England RL, et al. D-glucose stimulates mesangial cell GLUT1 expression and basal and IGF-I-sensitive glucose uptake in rat mesangial cells: implications for diabetic nephropathy. Diabetes 1997;46:1030-1039.
27. Gruden G, Thomas S, Burt D, et al. Mechanical stretch induces vascular permeability factor in human mesangial cells: mechanisms of signal transduction. Proc Natl Acad Sci USA 1997;94:12112-12116.
28. Schrijvers BF, Flyvbjerg A, Tilton RG, et al. Pathophysiological role of vascular endothelial growth factor in the remnant kidney. Nephron Exp Nephrol 2005;101:e9-e15.
29. Flyvbjerg A, Dagnaes-Hansen F, De Vriese AS, et al. Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody. Diabetes 2002;51:3090-3094.
30. Dunn SR, Qi Z, Bottinger EP, et al. Utility of endogenous creatinine clearance as a measure of renal function in mice. Kidney Int 2004;65:1959-1967.
31. Takemoto M, Asker N, Gerhardt H, et al. A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 2002;161:799-805.
32. Heilig CW, Saunders T, Brosius III FC, et al. Glucose transporter-1-deficient mice exhibit impaired development and deformities that are similar to diabetic embryopathy. Proc Natl Acad Sci USA 2003;100:15613- 15618.
33. Dumler F, Cortes P. Uracil ribonucleotide metabolism in rat and human glomerular epithelial and mesangial cells. Am J Physiol 1988;255:C712-C718.
34. Najafian B, Basgen JM, Mauer M. Estimating mean glomerular volume using two arbitrary parallel sections. J Am Soc Nephrol 2002;13:2697-2705.
35. Ivanyi B, Pap R, Ondrik Z. Thin basement membrane nephropathy: diffuse and segmental types. Arch Pathol Lab Med 2006;130: 1533-1537.
36. Stewart AD, Stewart J. Studies on syndrome of diabetes insipidus associated with oligosyndactyly in mice. Am J Physiol 1969;217: 1191-1198.
37. Sakai T, Kriz W. The structural relationship between mesangial cells and basement membrane of the renal glomerulus. Anat Embryol (Berl) 1987;176:373-386.
38. Lemley KV, Elger M, Koeppen-Hagemann I, et al. The glomerular mesangium: capillary support function and its failure under experimental conditions. Clin Invest 1992;70:843-856.
39. Pravtcheva DD, Wise TL. A transgene-induced mitotic arrest mutation in the mouse allelic with Oligosyndactylism. Genetics 1996;144: 1747-1756.
40. Chen RA, Scott S, Mattern WD, et al. The case for disease management in chronic kidney disease. Dis Manag 2006;9:86-92.
41. McClellan WM. The epidemic of renal disease-what drives it and what can be done? Nephrol Dial Transplant 2006;21:1461-1464.
42. Neuringer JR, Brenner BM. Glomerular hypertension: cause and consequence of renal injury. J Hypertens Suppl 1992;10:S91-S97.
43. Taal MW, Brenner BM. Combination ACEI and ARB therapy: additional benefit in renoprotection? Curr Opin Nephrol Hypertens 2002;11: 377-381.
44. Taal MW, Brenner BM. Achieving maximal renal protection in nondiabetic chronic renal disease. Am J Kidney Dis 2001;38:1365-1371.
45. Brenner BM, Zagrobelny J. Clinical renoprotection trials involving angiotensin II-receptor antagonists and angiotensin-converting-enzyme inhibitors. Kidney Int Suppl 2003;83:S77-S85.
46. Hostetter TH, Olson JL, Rennke HG, et al. Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation. Am J Physiol 1981;241:F85-F93.
47. Cheng H, Zhang M, Moeckel GW, et al. Expression of mediators of renal injury in the remnant kidney of ROP mice is attenuated by cyclooxygenase-2 inhibition. Nephron Exp Nephrol 2005;101:e75-e85.
48. Eremina V, Quaggin SE. The role of VEGF-A in glomerular development and function. Curr Opin Nephrol Hypertens 2004;13:9-15.
49. Henry DN, Busik JV, Brosius III FC, et al. Glucose transporters control gene expression of aldose reductase, PKCalpha, and GLUT1 in mesangial cells in vitro. Am J Physiol 1999;277:F97-104.
50. Weigert C, Brodbeck K, Brosius III FC, et al. Evidence for a novel TGF-beta1-independent mechanism of fibronectin production in mesangial cells overexpressing glucose transporters. Diabetes 2003;52:527-535.
51. Kumar A, Hawkins KS, Hannan MA, et al. Activation of PKC-beta(I) in glomerular mesangial cells is associated with specific NF-kappaB subunit translocation. Am J Physiol Renal Physiol 2002;281:F613-F619.
52. Heilig K, Chen S, Xiang M, et al. Overexpression of GLUT1 in glomeruli produces features of diabetic nephropathy (DN) in mice. (Abstr.). JASN 2004;15:263A.
53. Heilig CW, Brosius III FC, Henry DN. Glucose transporters of the glomerulus and the implications for diabetic nephropathy. Kidney Int 1997;60(Suppl):S91-S99.
54. Lenz T, Haak T, Malek J, et al. Vascular endothelial growth factor in diabetic nephropathy. Kidney Blood Press Res 2003;26:338-343.
55. Gruden G, Araf S, Zonca S, et al. IGF-I induces vascular endothelial growth factor in human mesangial cells via a Src-dependent mechanism. Kidney Int 2003;63:1249-1255.
56. Pfafflin A, Brodbeck K, Heilig CW, et al. Increased glucose uptake and metabolism in mesangial cells overexpressing glucose transporter 1 increases interleukin-6 and vascular endothelial growth factor production: role of AP-1 and HIF-1alpha. Cell Physiol Biochem 2006;18:199-210.
57. Kriz W, Elger M, Lemley K, et al. Structure of the glomerular mesangium: a biomechanical interpretation. Kidney Int 1990;30(Suppl):S2-S9.
58. Murakami T, Nishiyama T, Shirotani T, et al. Identification of two enhancer elements in the gene encoding the type 1 glucose transporter from the mouse which are responsive to serum, growth factor, and oncogenes. J Biol Chem 1992;267:9300-9306.
59. Kuusniemi AM, Merenmies J, Lahdenkari AT, et al. Glomerular sclerosis in kidneys with congenital nephrotic syndrome (NPHS1). Kidney Int 2006;70:1423-1431.
60. Eremina V, Sood M, Haigh J, et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 2003;111:707-716.