Renal accumulation of biglycan and lipid retention accelerates diabetic nephropathy

American Journal of Pathology

Volumn 179, Issue 3, 2011, Pages 1179-1187

  Thompson, Joel ^a,b   Wilson, Patricia ^a,b   Brandewie, Katie ^b   Taneja, Deepa ^b   Schaefer, Liliana ^c   Mitchell, Bonnie ^a   Tannock, Lisa R ^a,b  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; APOLIPOPROTEIN B; BIGLYCAN; DECORIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DIABETIC NEPHROPATHY; FEMALE; GLOMERULUS; HYPERLIPIDEMIA; KIDNEY HYPERTROPHY; LIPID STORAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; URINARY EXCRETION;

ALBUMINURIA; ANIMALS; APOLIPOPROTEINS B; BIGLYCAN; BLOTTING, WESTERN; CHOLESTEROL, DIETARY; DIABETIC NEPHROPATHIES; FEMALE; HYPERLIPIDEMIAS; KIDNEY; KIDNEY GLOMERULUS; LIPID METABOLISM; LIPOPROTEINS, LDL; MICE; MICE, INBRED C57BL; PROTEOGLYCANS; RECEPTORS, LDL;

EID: 80052864426     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.05.016     Document Type: Article

References (65)

1. H. Sato, S. Suzuki, H. Kobayashi, S. Ogino, A. Inomata, and M. Arakawa Immunohistological localization of lipoproteins in the glomeruli in renal disease: specifically apoB and apoE Clin Nephrol 36 1991 127 133
2. T. Takemura, K. Yoshioka, N. Aya, K. Murakami, A. Matumoto, H. Itakura, T. Kodama, H. Suzuki, and S. Maki lipoproteins and lipoprotein receptors in glomeruli in human kidney diseases Kidney Int 43 1993 918 927 (Pubitemid 23105228)
3. D.C. Wheeler, and R.S. Chana Interactions between lipoproteins, glomerular cells and matrix Miner Electrolyte Metab 19 1993 149 164 (Pubitemid 23305542)
4. H.S. Lee, J.S. Lee, H.I. Koh, and K.W. Ko Intraglomerular lipid deposition in routine biopsies Clin Nephrol 36 1991 67 75
5. A.F. Michael, W.F. Keane, L. Raij, R.L. Vernier, and S.M. Mauer The glomerular mesangium Kidney Int 17 1980 141 154 (Pubitemid 10095824)
6. J. Wasserman, A. Santiago, V. Rifici, H. Holthofer, L. Scharschmidt, M. Epstein, and D. Schlondorff Interactions of low density lipoprotein with rat mesangial cells Kidney Int 35 1989 1168 1174 (Pubitemid 19167904)
7. G. Coritsidis, V. Rifici, S. Gupta, J. Rie, Z.H. Shan, J. Neugarten, and D. Schlondorff Preferential binding of oxidized LDL to rat glomeruli in vivo and cultured mesangial cells in vitro Kidney Int 39 1991 858 866
8. J. Sano, S. Shirakura, S. Oda, T. Hara, and T. Ishihara Foam cells generated by a combination of hyperglycemia and hyperlipemia in rats Pathol Int 54 2004 904 913 (Pubitemid 40065081)
9. M.W. Spencer, A.S. Muhlfeld, S. Segerer, K.L. Hudkins, E. Kirk, R.C. LeBoeuf, and C.E. Alpers Hyperglycemia and hyperlipidemia act synergistically to induce renal disease in LDL receptor-deficient BALB mice Am J Nephrol 24 2004 20 31 (Pubitemid 38250483)
10. D. Taneja, J. Thompson, P. Wilson, K. Brandewie, L. Schaefer, B. Mitchell, and L.R. Tannock Reversibility of renal injury with cholesterol lowering in hyperlipidemic diabetic mice J Lipid Res 51 2010 1464 1470
11. V.S. Kamanna Low density lipoproteins and mitogenic signal transduction processes: role in the pathogenesis of renal disease Histol Histopathol 17 2002 497 505 (Pubitemid 34411209)
12. C.K. Abrass Cellular lipid metabolism and the role of lipids in progressive renal disease Am J Nephrol 24 2004 46 53 (Pubitemid 38258276)
13. V.S. Kamanna, D.D. Roh, and M.A. Kirschenbaum Hyperlipidemia and kidney disease: concepts derived from histopathology and cell biology of the glomerulus Histol Histopathol 13 1998 169 179 (Pubitemid 28044610)
14. K.J. Williams, and I. Tabas The response-to-retention hypothesis of early atherogenesis Arterioscler Thromb Vasc Biol 15 1995 551 561
15. I. Tabas, K.J. Williams, and J. Boren Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications Circulation 116 2007 1832 1844 (Pubitemid 350287108)
16. L.R. Tannock, and V.L. King Proteoglycan mediated lipoprotein retention: a mechanism of diabetic atherosclerosis Rev Endocr Metab Disord 9 2008 289 300
17. S.J. Hadad, Y.M. Michelacci, and N. Schor Proteoglycans and glycosaminoglycans synthesized in vitro by mesangial cells from normal and diabetic rats Biochim Biophys Acta 1290 1996 18 28 (Pubitemid 26174759)
18. S. Silbiger, D. Schlondorff, S. Crowley, L. Rosenberg, H. Choi, V. Hatcher, and P. Gordon The effect of glucose on proteoglycans produced by cultured mesangial cells Diabetes 42 1993 1815 1822 (Pubitemid 23346419)
19. F.N. Ziyadeh The extracellular matrix in diabetic nephropathy Am J Kidney Dis 22 1993 736 744 (Pubitemid 23330946)
20. L.R. Tannock Proteoglycans can mediate renal lipoprotein retention Diabetologia 49 2006 1115 1116
21. L. Schaefer, I. Raslik, H.J. Grone, E. Schonherr, K. Macakova, J. Ugorcakova, S. Budny, R.M. Schaefer, and H. Kresse Small proteoglycans in human diabetic nephropathy: discrepancy between glomerular expression and protein accumulation of decorin, biglycan, lumican, and fibromodulin FASEB J 15 2001 559 561
22. M.B. Stokes, S. Holler, Y. Cui, K.L. Hudkins, F. Eitner, A. Fogo, and C.E. Alpers Expression of decorin, biglycan, and collagen type I in human renal fibrosing disease Kidney Int 57 2000 487 498 (Pubitemid 30430640)
23. S. Merat, F. Casanada, M. Sutphin, W. Palinski, and P.D. Reaven Western-type diets induce insulin resistance and hyperinsulinemia in LDL receptor-deficient mice but do not increase aortic atherosclerosis compared with normoinsulinemic mice in which similar plasma cholesterol levels are achieved by a fructose-rich diet Arterioscler Thromb Vasc Biol 19 1999 1223 1230 (Pubitemid 29227641)
24. C.B. Renard, F. Kramer, F. Johansson, N. Lamharzi, L.R. Tannock, M.G. Herrath, A. Chait, and K.E. Bornfeldt Diabetes and diabetes-associated lipid abnormalities have distinct effects on initiation and progression of atherosclerotic lesions J Clin Invest 114 2004 659 668 (Pubitemid 39578756)
25. S. Taneda, J.W. Pippin, E.H. Sage, K.L. Hudkins, Y. Takeuchi, W.G. Couser, and C.E. Alpers Amelioration of diabetic nephropathy in SPARC-null mice J Am Soc Nephrol 14 2003 968 980 (Pubitemid 36359278)
26. F. Huang, J.C. Thompson, P.G. Wilson, H.H. Aung, J.C. Rutledge, and L.R. Tannock Angiotensin II increases vascular proteoglycan content preceding and contributing to atherosclerosis development J Lipid Res 49 2008 521 530
27. E. Schonherr, H.T. Jarvelainen, M.G. Kinsella, L.J. Sandell, and T.N. Wight Platelet derived growth factor and transforming growth factor-beta1 differentially affect the synthesis of biglycan and decorin by monkey arterial smooth muscle cells Arterioscler Thromb 13 1993 1026 1036 (Pubitemid 23195805)
28. L. Cai, A. Ji, F.C. de Beer, L.R. Tannock, and D.R. van der Westhuyzen SR-BI protects against endotoxemia in mice through its roles in glucocorticoid production and hepatic clearance J Clin Invest 118 2007 364 375
29. F.C. Brosius 3rd, C.E. Alpers, E.P. Bottinger, M.D. Breyer, T.M. Coffman, S.B. Gurley, R.C. Harris, M. Kakoki, M. Kretzler, E.H. Leiter, M. Levi, R.A. McIndoe, K. Sharma, O. Smithies, K. Susztak, N. Takahashi, and T. Takahashi Mouse models of diabetic nephropathy J Am Soc Nephrol 20 2009 2503 2512
30. T. Nakagawa, W. Sato, O. Glushakova, M. Heinig, T. Clarke, M. Campbell-Thompson, Y. Yuzawa, M.A. Atkinson, R.J. Johnson, and B. Croker Diabetic endothelial nitric oxide synthase knockout mice develop advanced diabetic nephropathy J Am Soc Nephrol 18 2007 539 550 (Pubitemid 46193319)
31. K.J. Williams, G. Qiu, H.K. Usui, S.R. Dunn, P. McCue, E. Bottinger, R.V. Iozzo, and K. Sharma Decorin deficiency enhances progressive nephropathy in diabetic mice Am J Pathol 171 2007 1441 1450 (Pubitemid 350158306)
32. S.J. Shankland, J.W. Scholey, H. Ly, and K. Thai Expression of transforming growth factor-beta 1 during diabetic renal hypertrophy Kidney Int 46 1994 430 442 (Pubitemid 24253050)
33. K. Sharma, and F.N. Ziyadeh Renal hypertrophy is associated with upregulation of TGF-beta 1 gene expression in diabetic BB rat and NOD mouse Am J Physiol 267 1994 F1094-F1001
34. T. Yamamoto, T. Nakamura, N.A. Noble, E. Ruoslahti, and W.A. Border Expression of transforming growth factor beta is elevated in human and experimental diabetic nephropathy Proc Natl Acad Sci U S A 90 1993 1814 1818 (Pubitemid 23069947)
35. P.J. Little, L. Tannock, K.L. Olin, A. Chait, and T.N. Wight Proteoglycans synthesized by arterial smooth muscle cells in the presence of transforming growth factor-beta1 exhibit increased binding to LDLs Arterioscler Thromb Vasc Biol 22 2002 55 60 (Pubitemid 34076232)
36. A.S. Muhlfeld, M.W. Spencer, K.L. Hudkins, E. Kirk, R.C. LeBoeuf, and C.E. Alpers Hyperlipidemia aggravates renal disease in B6.ROP Os/+ mice Kidney Int 66 2004 1393 1402 (Pubitemid 39298371)
37. M. Ravid, D. Brosh, D. Ravid-Safran, Z. Levy, and R. Rachmani Main risk factors for nephropathy in type 2 diabetes mellitus are plasma cholesterol levels, mean blood pressure, and hyperglycemia Arch Intern Med 158 1998 998 1004 (Pubitemid 28213577)
38. O. Samuelsson, H. Mulec, C. Knight-Gibson, P.O. Attman, B. Kron, R. Larsson, L. Weiss, H. Wedel, and P. Alaupovic Lipoprotein abnormalities are associated with increased rate of progression of human chronic renal insufficiency Nephrol Dial Transplant 12 1997 1908 1915 (Pubitemid 27379464)
39. M. Wen, S. Segerer, M. Dantas, P.A. Brown, K.L. Hudkins, T. Goodpaster, E. Kirk, R.C. LeBoeuf, and C.E. Alpers Renal injury in lipoprotein E-deficient mice Lab Invest 82 2002 999 1006
40. S. Fazio, and M.F. Linton Mouse models of hyperlipidemia and atherosclerosis Front Biosci 6 2001 D515 D525
41. K. Sharma, Y. Jin, J. Guo, and F.N. Ziyadeh 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 1996 522 530
42. F.N. Ziyadeh, B.B. Hoffman, D.C. Han, M.C. Iglesias-De La Cruz, S.W. Hong, M. Isono, S. Chen, T.A. McGowan, and K. Sharma 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 U S A 97 2000 8015 8020 (Pubitemid 30460765)
43. W.A. Border, S. Okuda, L.R. Languino, and E. Ruoslahti Transforming growth factor-beta regulates production of proteoglycans by mesangial cells Kidney Int 37 1990 689 695 (Pubitemid 20056841)
44. M.M. Mozes, E.P. Bottinger, T.A. Jacot, and J.B. Kopp Renal expression of fibrotic matrix proteins and of transforming growth factor-beta (TGF-beta) isoforms in TGF-beta transgenic mice J Am Soc Nephrol 10 1999 271 280 (Pubitemid 29068066)
45. H. Ungefroren, W. Lenschow, W.B. Chen, F. Faendrich, and H. Kalthoff Regulation of biglycan gene expression by transforming growth factor-beta requires MKK6-p38 mitogen-activated protein Kinase signaling downstream of Smad signaling J Biol Chem 278 2003 11041 11049 (Pubitemid 36792654)
46. P. Wilson, K. Drennon, and L.R. Tannock Regulation of vascular proteoglycan synthesis by metabolic factors associated with diabetes J Investig Med 55 2007 18 25 (Pubitemid 46512738)
47. R.A. Page, and A.N. Malik Elevated levels of beta defensin-1 mRNA in diabetic kidneys of GK rats Biochem Biophys Res Commun 310 2003 513 521 (Pubitemid 37163694)
48. A. Bjornson, J. Moses, A. Ingemansson, B. Haraldsson, and J. Sorensson Primary human glomerular endothelial cells produce proteoglycans, and puromycin affects their posttranslational modification Am J Physiol Renal Physiol 288 2005 F748 F756
49. A. Bjornson Granqvist, K. Ebefors, M.A. Saleem, P.W. Mathieson, B. Haraldsson, and J.S. Nystrom Podocyte proteoglycan synthesis is involved in the development of nephrotic syndrome Am J Physiol Renal Physiol 291 2006 F722 F730
50. L. Schaefer, K.F. Beck, I. Raslik, S. Walpen, D. Mihalik, M. Micegova, K. Macakova, E. Schonherr, D.G. Seidler, G. Varga, R.M. Schaefer, H. Kresse, and J. Pfeilschifter Biglycan, a nitric oxide-regulated gene, affects adhesion, growth, and survival of mesangial cells J Biol Chem 278 2003 26227 26237 (Pubitemid 36835392)
51. W.A. Border, N.A. Noble, T. Yamamoto, J.R. Harper, Y. Yamaguchi, M.D. Pierschbacher, and E. Ruoslahti Natural inhibitor of transforming growth factor-beta protects against scarring in experimental kidney disease Nature 360 1992 361 364 (Pubitemid 23000677)
52. A. Babelova, K. Moreth, W. Tsalastra-Greul, J. Zeng-Brouwers, O. Eickelberg, M.F. Young, P. Bruckner, J. Pfeilschifter, R.M. Schaefer, H.J. Grone, and L. Schaefer Biglycan, a danger signal that activates the NLRP3 inflammasome via Toll-like and P2X receptors J Biol Chem 284 2009 24035 24048
53. L. Schaefer, D. Mihalik, A. Babelova, M. Krzyzankova, H.J. Grone, R.V. Iozzo, M.F. Young, D.G. Seidler, G. Lin, D.P. Reinhardt, and R.M. Schaefer Regulation of fibrillin-1 by biglycan and decorin is important for tissue preservation in the kidney during pressure-induced injury Am J Pathol 165 2004 383 396 (Pubitemid 38971370)
54. A. Hildebrand, M. Romaris, L.M. Rasmussen, D. Heinegard, D.R. Twardzik, W.A. Border, and E. Ruoslahti Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta Biochem J 302 Pt 2 1994 527 534 (Pubitemid 24280108)
55. Y. Yamaguchi, D.M. Mann, and E. Ruoslahti Negative regulation of transforming growth factor-beta by the proteoglycan decorin Nature 346 1990 281 284
56. W. Huijun, C. Long, Z. Zhigang, J. Feng, and G. Muyi Ex vivo transfer of the decorin gene into rat glomerulus via a mesangial cell vector suppressed extracellular matrix accumulation in experimental glomerulonephritis Exp Mol Pathol 78 2005 17 24 (Pubitemid 41373312)
57. M. Kolb, P.J. Margetts, P.J. Sime, and J. Gauldie Proteoglycans decorin and biglycan differentially modulate TGF-beta-mediated fibrotic responses in the lung Am J Physiol Lung Cell Mol Physiol 280 2001 L1327 L1334
58. A. Mogyorosi, and F.N. Ziyadeh Increased decorin mRNA in diabetic mouse kidney and in mesangial and tubular cells cultured in high glucose Am J Physiol 275 1998 F827 F832
59. S.B. Gurley, S.E. Clare, K.P. Snow, A. Hu, T.W. Meyer, and T.M. Coffman Impact of genetic background on nephropathy in diabetic mice Am J Physiol Renal Physiol 290 2006 F214 F222
60. Z. Qi, H. Fujita, J. Jin, L.S. Davis, Y. Wang, A.B. Fogo, and M.D. Breyer Characterization of susceptibility of inbred mouse strains to diabetic nephropathy Diabetes 54 2005 2628 2637 (Pubitemid 41233584)
61. Y.C. Tay, Y. Wang, L. Kairaitis, G.K. Rangan, C. Zhang, and D.C. Harris Can murine diabetic nephropathy be separated from superimposed acute renal failure? Kidney Int 68 2005 391 398 (Pubitemid 43181399)
62. Prevention of cardiovascular events and death with pravastatin in patients with coronary heart disease and a broad range of initial cholesterol levels The Long-Term Intervention with Pravastatin in Ischaemic Disease (LIPID) Study Group N Engl J Med 339 1998 1349 1357
63. MRC/BHF Heart Protection Study of cholesterol lowering with simvastatin in 20,536 high-risk individuals: a randomised placebo-controlled trial Lancet 360 2002 7 22
64. Major outcomes in moderately hypercholesterolemic, hypertensive patients randomized to pravastatin vs usual care: The Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial (ALLHAT-LLT) JAMA 288 2002 2998 3007
65. B.C. Fellstrom, A.G. Jardine, R.E. Schmieder, H. Holdaas, K. Bannister, J. Beutler, D.W. Chae, A. Chevaile, S.M. Cobbe, C. Gronhagen-Riska, J.J. De Lima, R. Lins, G. Mayer, A.W. McMahon, H.H. Parving, G. Remuzzi, O. Samuelsson, S. Sonkodi, D. Sci, G. Suleymanlar, D. Tsakiris, V. Tesar, V. Todorov, A. Wiecek, R.P. Wuthrich, M. Gottlow, E. Johnsson, and F. Zannad Rosuvastatin and cardiovascular events in patients undergoing hemodialysis N Engl J Med 360 2009 1395 1407