Transgenic overexpression of GLUT1 in mouse glomeruli produces renal disease resembling diabetic glomerulosclerosis

American Journal of Physiology - Renal Physiology

Volumn 299, Issue 1, 2010, Pages

  Wang, Youli ^a   Heilig, Kathleen ^a,b   Saunders, Thomas ^c   Minto, Andrew ^a   Deb, Dilip K ^a   Chang, Anthony ^a   Brosius, Frank ^c   Monteiro, Carmela ^d   Heilig, Charles W ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

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

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

Diabetic nephropathy; Transgene; VEGF

Indexed keywords

COLLAGEN TYPE 4; FIBRONECTIN; GLUCOSE; GLUCOSE TRANSPORTER 1; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MATRIX PROTEIN; PROTEIN KINASE C; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD PRESSURE; CAPILLARY; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DISEASE SEVERITY; ENZYME ACTIVATION; GENE OVEREXPRESSION; GLOMERULUS; GLOMERULUS BASEMENT MEMBRANE; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; INTRACELLULAR SIGNALING; KIDNEY BLOOD VESSEL; KIDNEY DISEASE; KIDNEY TUBULE; MESANGIUM CELL; MOUSE; NONHUMAN; ORGAN WEIGHT; PODOCYTE; PRIORITY JOURNAL; TRANSGENIC MOUSE;

EID: 77953833285     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00466.2009     Document Type: Article

References (53)

1. Bao Y, Jia RH, Yuan J, Li J. Rosiglitazone ameliorates diabetic nephropathy by inhibiting reactive oxygen species and its downstream-signaling pathways. Pharmacology 80: 57-64, 2007. (Pubitemid 47013368)
2. Chen SH, Brosius F 3rd, Heilig C. Diabetes increases glomerular GLUT1, and antisense-GLUT1 protects against diabetic glomerulosclerosis (Abstract). JASN 14: 14A, 2003.
3. Chen S, Mukherjee S, Chakraborty C, Chakrabarti S. High glucoseinduced, endothelin-dependent fibronectin synthesis is mediated via NF-κB and AP-1. Am J Physiol Cell Physiol 284: C263-C272, 2003.
4. Chin E, Zamah AM, Landau D, Gronbcek H, Flyvbjerg A, LeRoith D, Bondy CA. Changes in facilitative glucose transporter messenger ribonucleic acid levels in the diabetic rat kidney. Endocrinology 138: 1267-1275, 1997. (Pubitemid 27089786)
5. Cortes P, Mendez M, Riser BL, Guerin CJ, Rodriguez-Barbero A, Hassett C, Yee J. F-actin fiber distribution in glomerular cells: structural and functional implications. Kidney Int 58: 2452-2461, 2000.
6. D'Agord Schaan B, Lacchini S, Bertoluci MC, Irigoyen MC, Machado UF, Schmid H. Increased renal GLUT1 abundance and urinary TGF-beta 1 in streptozotocin-induced diabetic rats: implications for the development of nephropathy complicating diabetes. Horm Metab Res 33: 664-669, 2001. (Pubitemid 33151465)
7. Derubertis FR, Craven PA. Activation of protein kinase C in glomerular cells in diabetes. Mechanisms and potential links to the pathogenesis of diabetic glomerulopathy. Diabetes 43: 1-8, 1994. (Pubitemid 24010522)
8. de Vriese AS, Tilton RG, Elger M, Stephan CC, Kriz W, Lameire NH. Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes. J Am Soc Nephrol 12: 993-1000, 2001. (Pubitemid 32378340)
9. 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-dependent diabetes mellitus. N Engl J Med 329: 977-986, 1993.
10. Dominguez JH, Camp K, Maianu L, Feister H, Garvey WT. Molecular adaptations of GLUT1 and GLUT2 in renal proximal tubules of diabetic rats. Am J Physiol Renal Fluid Electrolyte Physiol 266: F283-F290, 1994. (Pubitemid 24104759)
11. Dumler F, Cortes P. Uracil ribonucleotide metabolism in rat and human glomerular epithelial and mesangial cells. Am J Physiol Cell Physiol 255: C712-C718, 1988. (Pubitemid 19025704)
12. Dunn SR, Qi Z, Bottinger EP, Breyer MD, Sharma K. Utility of endogenous creatinine clearance as a measure of renal function in mice. Kidney Int 65: 1959-1967, 2004.
13. Flyvbjerg A, Dagnaes-Hansen F, De Vriese AS, Schrijvers BF, Tilton RG, Rasch R. Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody. Diabetes 51: 3090-3094, 2002.
14. Gnudi L, Viberti G, Raij L, Rodriguez V, Burt D, Cortes P, Hartley B, Thomas S, Maestrini S, Gruden G. GLUT-1 overexpression: link between hemodynamic and metabolic factors in glomerular injury? Hypertension 42: 19-24, 2003.
15. Gunning P, Leavitt J, Muscat G, Ng SY, Kedes L. A human beta-actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci USA 84: 4831-4835, 1987.
16. Ha H, Lee HB. Reactive oxygen species amplify glucose signalling in renal cells cultured under high glucose and in diabetic kidney. Nephrology (Carlton) 10, Suppl 2: S7-S10, 2005.
17. Ha H, Lee HB. Reactive oxygen species as glucose signaling molecules in mesangial cells cultured under high glucose. Kidney Int Suppl 77: S19-S25, 2000.
18. Ha H, Yu MR, Choi YJ, Kitamura M, Lee HB. Role of high glucose-induced nuclear factor-kappaB activation in monocyte chemoattractant protein-1 expression by mesangial cells. J Am Soc Nephrol 13: 894-902, 2002.
19. Heilig CW, Concepcion LA, Riser BL, Freytag SO, Zhu M, Cortes P. Overexpression of glucose transporters in rat mesangial cells cultured in a normal glucose milieu mimics the diabetic phenotype. J Clin Invest 96: 1802-1814, 1995.
20. Heilig CW, Kreisberg JI, Freytag S, Murakami T, Ebina Y, Guo L, Heilig K, Loberg R, Qu X, Jin Y, Henry D, Brosius FC 3rd. Antisense GLUT-1 protects mesangial cells from glucose induction of GLUT-1 and fibronectin expression. Am J Physiol Renal Physiol 280: F657-F666, 2001.
21. Heilig CW, Liu Y, England RL, Freytag SO, Gilbert JD, Heilig KO, Zhu M, Concepcion LA, Brosius FC 3rd. D-Glucose stimulates mesangial cell GLUT1 expression and basal and IGF-I-sensitive glucose uptake in rat mesangial cells: implications for diabetic nephropathy. Diabetes 46: 1030-1039, 1997.
22. Heilig K, Chen S, Xiang M, Brosius F, Heilig C. Overexpression of GLUT1 in glomeruli produces features of diabetic nephropathy (DN) in mice (Abstract). JASN 15: 263A, 2004.
23. Henry DN, Busik JV, Brosius FC 3rd, Heilig CW. Glucose transporters control gene expression of aldose reductase, PKCα, and GLUT1 in mesangial cells in vitro. Am J Physiol Renal Physiol 277: F97-F104, 1999.
24. 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.
25. Inoki K, Haneda M, Maeda S, Koya D, Kikkawa R. TGF-beta 1 stimulates glucose uptake by enhancing GLUT1 expression in mesangial cells. Kidney Int 55: 1704-1712, 1999.
26. Kanesaki Y, Suzuki D, Uehara G, Toyoda M, Katoh T, Sakai H, Watanabe T. Vascular endothelial growth factor gene expression is correlated with glomerular neovascularization in human diabetic nephropathy. Am J Kidney Dis 45: 288-294, 2005.
27. Kirkpatrick JC, Heilig K, Wang Y, Lammertin G, Schlimme M, Hall J, Quigg R, Lang R, Heilig C. Cardiac hypertrophy and renal disease in GLUT1-overexpressing mice (Abstract). JACC 918: 38A, 2006.
28. Kriz W, Elger M, Lemley K, Sakai T. Structure of the glomerular mesangium: a biomechanical interpretation. Kidney Int Suppl 30: S2-S9, 1990.
29. I in glomerular mesangial cells is associated with specific NF-κB subunit translocation. Am J Physiol Renal Physiol 281: F613-F619, 2001.
30. Lenz T, Haak T, Malek J, Grone HJ, Geiger H, Gossmann J. Vascular endothelial growth factor in diabetic nephropathy. Kidney Blood Press Res 26: 338-343, 2003. (Pubitemid 37465042)
31. Linden KC, DeHaan CL, Zhang Y, Glowacka S, Cox AJ, Kelly DJ, Rogers S. Renal expression and localization of the facilitative glucose transporters GLUT1 and GLUT12 in animal models of hypertension and diabetic nephropathy. Am J Physiol Renal Physiol 290: F205-F213, 2006.
32. Marks J, Carvou NJ, Debnam ES, Srai SK, Unwin RJ. Diabetes increases facilitative glucose uptake and GLUT2 expression at the rat proximal tubule brush border membrane. J Physiol 553: 137-145, 2003. (Pubitemid 37483922)
33. Najafian B, Basgen JM, Mauer M. Estimating mean glomerular volume using two arbitrary parallel sections. J Am Soc Nephrol 13: 2697-2705, 2002. (Pubitemid 35216038)
34. Nishikawa T, Edelstein D, Brownlee M. The missing link: a single unifying mechanism for diabetic complications. Kidney Int Suppl 77: S26-S30, 2000.
35. Ohga S, Shikata K, Yozai K, Okada S, Ogawa D, Usui H, Wada J, Shikata Y, Makino H. Thiazolidinedione ameliorates renal injury in experimental diabetic rats through anti-inflammatory effects mediated by inhibition of NF-κB activation. Am J Physiol Renal Physiol 292: F1141-F1150, 2007. (Pubitemid 46578056)
36. Pfafflin A, Brodbeck K, Heilig CW, Haring HU, Schleicher ED, Weigert C. 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 18: 199-210, 2006. (Pubitemid 44946976)
37. Ricci C, Iacobini C, Oddi G, Amadio L, Menini S, Rastaldi MP, Frasheri A, Pricci F, Pugliese F, Pugliese G. Role of TGF-beta/GLUT1 axis in susceptibility vs resistance to diabetic glomerulopathy in the Milan rat model. Nephrol Dial Transplant 21: 1514-1524, 2006.
38. Sakai T, Kriz W. The structural relationship between mesangial cells and basement membrane of the renal glomerulus. Anat Embryol (Berl) 176: 373-386, 1987.
39. Schrijvers BF, Flyvbjerg A, De Vriese AS. The role of vascular endothelial growth factor (VEGF) in renal pathophysiology. Kidney Int 65: 2003-2017, 2004.
40. Schrijvers BF, Flyvbjerg A, Tilton RG, Lameire NH, De Vriese AS. A neutralizing VEGF antibody prevents glomerular hypertrophy in a model of obese type 2 diabetes, the Zucker diabetic fatty rat. Nephrol Dial Transplant 21: 324-329, 2006.
41. Sharma K, Jin Y, Guo J, Ziyadeh FN. Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 45: 522-530, 1996.
42. Studer RK, Craven PA, DeRubertis FR. Role for protein kinase C in the mediation of increased fibronectin accumulation by mesangial cells grown in high-glucose medium. Diabetes 42: 118-126, 1993.
43. Sugaru E, Nakagawa T, Ono-Kishino M, Nagamine J, Tokunaga T, Kitoh M, Hume WE, Nagata R, Taiji M. Amelioration of established diabetic nephropathy by combined treatment with SMP-534 (antifibrotic agent) and losartan in db/db mice. Nephron Exp Nephrol 105: e45-e52, 2007.
44. 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.
45. Thomas MC, Burns WC, Cooper ME. Tubular changes in early diabetic nephropathy. Adv Chronic Kidney Dis 12: 177-186, 2005.
46. UK Prospective Diabetes Study Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352: 837-853, 1998.
47. Vesely ED, Heilig CW, Brosius FC 3rd. GLUT1-induced cFLIP expression promotes proliferation and prevents apoptosis in vascular smooth muscle cells. Am J Physiol Cell Physiol 297: C759-C765, 2009.
48. Wang Y, Heilig KO, Minto AW, Chen S, Xiang M, Dean DA, Geiger RC, Chang A, Pravtcheva DD, Schlimme M, Deb DK, Heilig CW. Nephron-deficient Fvb mice develop rapidly progressive renal failure and heavy albuminuria involving excess glomerular GLUT1 and VEGF. Lab Invest 90: 83-97, 2010.
49. Weigert C, Brodbeck K, Brosius FC 3rd, Huber M, Lehmann R, Friess U, Facchin S, Aulwurm S, Haring HU, Schleicher ED, Heilig CW. Evidence for a novel TGF-beta1-independent mechanism of fibronectin production in mesangial cells overexpressing glucose transporters. Diabetes 52: 527-535, 2003.
50. Xiang MHK, Heilig C. TGF-β1 and PKC activate GLUT1 transcription in mesangial cells (MC) via separate regulatory sites (Abstract). JASN 15: 466A, 2004.
51. Yasuda T, Imai H, Nakamoto Y, Miura AB, Inomata S. Significance of fibrils in the formation of the Kimmelstiel-Wilson nodule. Virchows Arch A Pathol Anat Histopathol 421: 297-303, 1992.
52. Ziyadeh FN. Mediators of diabetic renal disease: the case for tgf-beta as the major mediator. J Am Soc Nephrol 15, Suppl 1: S55-S57, 2004.
53. Ziyadeh FN, Hoffman BB, Han DC, Iglesias-De La Cruz MC, Hong SW, Isono M, Chen S, McGowan TA, Sharma K. Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc Natl Acad Sci USA 97: 8015-8020, 2000.