Heparanase is essential for the development of acute experimental glomerulonephritis

American Journal of Pathology

Volumn 186, Issue 4, 2016, Pages 805-815

  Garsen, Marjolein ^a   Benner, Marilen ^a   Dijkman, Henry B ^a   Van Kuppevelt, Toin H ^a   Li, Jin Ping ^b   Rabelink, Ton J ^c   Vlodavsky, Israel ^d   Berden, Jo H M ^a   Rops, Angelique L W M M ^a   Elkin, Michael ^e   Van Der Vlag, Johan ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UPPSALA UNIVERSITY   (Sweden)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; GAMMA INTERFERON; HEPARANASE; INTERLEUKIN 10; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; SYNDECAN 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; BETA GLUCURONIDASE; HEPARAN SULFATE; TUMOR NECROSIS FACTOR;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; EXPERIMENTAL GLOMERULONEPHRITIS; GLOMERULUS BASEMENT MEMBRANE; IN VITRO STUDY; INFLAMMATORY CELL; KIDNEY CORTEX; KIDNEY FUNCTION; KIDNEY INJURY; LEUKOCYTE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; TH1 CELL; TH2 CELL; WILD TYPE; ACUTE DISEASE; ANIMAL; C57BL MOUSE; DIABETIC NEPHROPATHY; GLOMERULONEPHRITIS; METABOLISM;

ACUTE DISEASE; ANIMALS; DIABETIC NEPHROPATHIES; GLOMERULAR BASEMENT MEMBRANE; GLOMERULONEPHRITIS; GLUCURONIDASE; HEPARITIN SULFATE; MICE, INBRED C57BL; PROTEINURIA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84962613993     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.12.008     Document Type: Article

References (51)

1. K. Tryggvason, and E. Pettersson Causes and consequences of proteinuria: the kidney filtration barrier and progressive renal failure J Intern Med 254 2003 216 224
2. Y.S. Kanwar, and M.G. Farquhar Presence of heparan sulfate in the glomerular basement membrane Proc Natl Acad Sci U S A 76 1979 1303 1307
3. M. Garsen, A.L. Rops, T.J. Rabelink, J.H. Berden, and J. van der Vlag The role of heparanase and the endothelial glycocalyx in the development of proteinuria Nephrol Dial Transplant 29 2014 49 55
4. Y.S. Kanwar, and M.G. Farquhar Isolation of glycosaminoglycans (heparan sulfate) from glomerular basement membranes Proc Natl Acad Sci U S A 76 1979 4493 4497
5. G.C. Groggel, J. Stevenson, P. Hovingh, A. Linker, and W.A. Border Changes in heparan sulfate correlate with increased glomerular permeability Kidney Int 33 1988 517 523
6. Y.S. Kanwar, A. Linker, and M.G. Farquhar Increased permeability of the glomerular basement membrane to ferritin after removal of glycosaminoglycans (heparan sulfate) by enzyme digestion J Cell Biol 86 1980 688 693
7. M.J. van den Hoven, T.J. Wijnhoven, J.P. Li, E. Zcharia, H.B. Dijkman, R.G. Wismans, A.L. Rops, J.F. Lensen, L.P. van den Heuvel, T.H. van Kuppevelt, I. Vlodavsky, J.H. Berden, and J. van der Vlag Reduction of anionic sites in the glomerular basement membrane by heparanase does not lead to proteinuria Kidney Int 73 2008 278 287
8. S.J. Harvey, G. Jarad, J. Cunningham, A.L. Rops, J. van der Vlag, J.H. Berden, M.J. Moeller, L.B. Holzman, R.W. Burgess, and J.H. Miner Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity Am J Pathol 171 2007 139 152
9. S. Chen, D.J. Wassenhove-McCarthy, Y. Yamaguchi, L.B. Holzman, T.H. van Kuppevelt, G.J. Jenniskens, T.J. Wijnhoven, A.C. Woods, and K.J. McCarthy Loss of heparan sulfate glycosaminoglycan assembly in podocytes does not lead to proteinuria Kidney Int 74 2008 289 299
10. J. van den Born, L.P. van den Heuvel, M.A. Bakker, J.H. Veerkamp, K.J. Assmann, J.J. Weening, and J.H. Berden Distribution of GBM heparan sulfate proteoglycan core protein and side chains in human glomerular diseases Kidney Int 43 1993 454 463
11. A.L. Rops, J. van der Vlag, J.F. Lensen, T.J. Wijnhoven, L.P. van den Heuvel, T.H. van Kuppevelt, and J.H. Berden Heparan sulfate proteoglycans in glomerular inflammation Kidney Int 65 2004 768 785
12. S. Sarrazin, W.C. Lamanna, and J.D. Esko Heparan sulfate proteoglycans Cold Spring Harb Perspect Biol 3 2011 pii: a004952
13. A.L. Rops, M.J. van den Hoven, M.M. Baselmans, J.F. Lensen, T.J. Wijnhoven, L.P. van den Heuvel, T.H. van Kuppevelt, J.H. Berden, and J. van der Vlag Heparan sulfate domains on cultured activated glomerular endothelial cells mediate leukocyte trafficking Kidney Int 73 2008 52 62
14. M.J. van den Hoven, A.L. Rops, I. Vlodavsky, V. Levidiotis, J.H. Berden, and J. van der Vlag Heparanase in glomerular diseases Kidney Int 72 2007 543 548
15. G. Abboud-Jarrous, R. Atzmon, T. Peretz, C. Palermo, B.B. Gadea, J.A. Joyce, and I. Vlodavsky Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment J Biol Chem 283 2008 18167 18176
16. N. Ilan, M. Elkin, and I. Vlodavsky Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis Int J Biochem Cell Biol 38 2006 2018 2039
17. Y. Yang, V. Macleod, M. Bendre, Y. Huang, A.M. Theus, H.Q. Miao, P. Kussie, S. Yaccoby, J. Epstein, L.J. Suva, T. Kelly, and R.D. Sanderson Heparanase promotes the spontaneous metastasis of myeloma cells to bone Blood 105 2005 1303 1309
18. C.R. Parish, C. Freeman, and M.D. Hulett Heparanase: a key enzyme involved in cell invasion Biochim Biophys Acta 1471 2001 M99 M108
19. E.P. Schmidt, Y. Yang, W.J. Janssen, A. Gandjeva, M.J. Perez, L. Barthel, R.L. Zemans, J.C. Bowman, D.E. Koyanagi, Z.X. Yunt, L.P. Smith, S.S. Cheng, K.H. Overdier, K.R. Thompson, M.W. Geraci, I.S. Douglas, D.B. Pearse, and R.M. Tuder The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis Nat Med 18 2012 1217 1223
20. R.W. Li, C. Freeman, D. Yu, E.J. Hindmarsh, K.E. Tymms, C.R. Parish, and P.N. Smith Dramatic regulation of heparanase activity and angiogenesis gene expression in synovium from patients with rheumatoid arthritis Arthritis Rheum 58 2008 1590 1600
21. P.E. Brenchley Antagonising angiogenesis in rheumatoid arthritis Ann Rheum Dis 60 Suppl 3 2001 iii71 iii74
22. I. Lerner, E. Hermano, E. Zcharia, D. Rodkin, R. Bulvik, V. Doviner, A.M. Rubinstein, R. Ishai-Michaeli, R. Atzmon, Y. Sherman, A. Meirovitz, T. Peretz, I. Vlodavsky, and M. Elkin Heparanase powers a chronic inflammatory circuit that promotes colitis-associated tumorigenesis in mice J Clin Invest 121 2011 1709 1721
23. N. Gil, R. Goldberg, T. Neuman, M. Garsen, E. Zcharia, A.M. Rubinstein, T. van Kuppevelt, A. Meirovitz, C. Pisano, J.P. Li, J. van der Vlag, I. Vlodavsky, and M. Elkin Heparanase is essential for the development of diabetic nephropathy in mice Diabetes 61 2012 208 216
24. R. Goldberg, A.M. Rubinstein, N. Gil, E. Hermano, J.P. Li, J. van der Vlag, R. Atzmon, A. Meirovitz, and M. Elkin Role of heparanase-driven inflammatory cascade in pathogenesis of diabetic nephropathy Diabetes 63 2014 4302 4313
25. V. Levidiotis, C. Freeman, C. Tikellis, M.E. Cooper, and D.A. Power Heparanase is involved in the pathogenesis of proteinuria as a result of glomerulonephritis J Am Soc Nephrol 15 2004 68 78
26. V. Levidiotis, C. Freeman, M. Punler, P. Martinello, B. Creese, V. Ferro, J. van der Vlag, J.H. Berden, C.R. Parish, and D.A. Power A synthetic heparanase inhibitor reduces proteinuria in passive Heymann nephritis J Am Soc Nephrol 15 2004 2882 2892
27. V. Levidiotis, C. Freeman, C. Tikellis, M.E. Cooper, and D.A. Power Heparanase inhibition reduces proteinuria in a model of accelerated anti-glomerular basement membrane antibody disease Nephrology (Carlton) 10 2005 167 173
28. C. Xu, A. Chang, B.K. Hack, M.T. Eadon, S.L. Alper, and P.N. Cunningham TNF-mediated damage to glomerular endothelium is an important determinant of acute kidney injury in sepsis Kidney Int 85 2014 72 81
29. M.I. Lygizos, Y. Yang, C.J. Altmann, K. Okamura, A.A. Hernando, M.J. Perez, L.P. Smith, D.E. Koyanagi, A. Gandjeva, R. Bhargava, R.M. Tuder, S. Faubel, and E.P. Schmidt Heparanase mediates renal dysfunction during early sepsis in mice Physiol Rep 1 2013 e00153
30. E. Zcharia, J. Jia, X. Zhang, L. Baraz, U. Lindahl, T. Peretz, I. Vlodavsky, and J.P. Li Newly generated heparanase knock-out mice unravel co-regulation of heparanase and matrix metalloproteinases PLoS One 4 2009 e5181
31. A.L. Rops, M. Gotte, M.H. Baselmans, M.J. van den Hoven, E.J. Steenbergen, J.F. Lensen, T.J. Wijnhoven, F. Cevikbas, L.P. van den Heuvel, T.H. van Kuppevelt, J.H. Berden, and J. van der Vlag Syndecan-1 deficiency aggravates anti-glomerular basement membrane nephritis Kidney Int 72 2007 1204 1215
32. E.M. van de Westerlo, T.F. Smetsers, M.A. Dennissen, R.J. Linhardt, J.H. Veerkamp, G.N. van Muijen, and T.H. van Kuppevelt Human single chain antibodies against heparin: selection, characterization, and effect on coagulation Blood 99 2002 2427 2433
33. C.J. Raats, M.A. Bakker, W. Hoch, W.P. Tamboer, A.J. Groffen, L.P. van den Heuvel, J.H. Berden, and J. van den Born Differential expression of agrin in renal basement membranes as revealed by domain-specific antibodies J Biol Chem 273 1998 17832 17838
34. A.L. Rops, J. van der Vlag, C.W. Jacobs, H.B. Dijkman, J.F. Lensen, T.J. Wijnhoven, L.P. van den Heuvel, T.H. van Kuppevelt, and J.H. Berden Isolation and characterization of conditionally immortalized mouse glomerular endothelial cell lines Kidney Int 66 2004 2193 2201
35. P. Mundel, J. Reiser, A. Zuniga Mejia Borja, H. Pavenstadt, G.R. Davidson, W. Kriz, and R. Zeller Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines Exp Cell Res 236 1997 248 258
36. A.L. Rops, M.A. Loeven, J.J. van Gemst, I. Eversen, X.M. Van Wijk, H.B. Dijkman, T.H. van Kuppevelt, J.H. Berden, T.J. Rabelink, J.D. Esko, and J. van der Vlag Modulation of heparan sulfate in the glomerular endothelial glycocalyx decreases leukocyte influx during experimental glomerulonephritis Kidney Int 86 2014 932 942
37. K.J. Assmann, M.M. Tangelder, W.P. Lange, G. Schrijver, and R.A. Koene Anti-GBM nephritis in the mouse: severe proteinuria in the heterologous phase Virchows Arch A Pathol Anat Histopathol 406 1985 285 299
38. V.C. Ramani, A. Purushothaman, M.D. Stewart, C.A. Thompson, I. Vlodavsky, J.L. Au, and R.D. Sanderson The heparanase/syndecan-1 axis in cancer: mechanisms and therapies FEBS J 280 2013 2294 2306
39. A. Purushothaman, T. Uyama, F. Kobayashi, S. Yamada, K. Sugahara, A.C. Rapraeger, and R.D. Sanderson Heparanase-enhanced shedding of syndecan-1 by myeloma cells promotes endothelial invasion and angiogenesis Blood 115 2010 2449 2457
40. Y. Yang, V. Macleod, H.Q. Miao, A. Theus, F. Zhan, J.D. Shaughnessy Jr., J. Sawyer, J.P. Li, E. Zcharia, I. Vlodavsky, and R.D. Sanderson Heparanase enhances syndecan-1 shedding: a novel mechanism for stimulation of tumor growth and metastasis J Biol Chem 282 2007 13326 13333
41. K. Asanuma, K. Kim, J. Oh, L. Giardino, S. Chabanis, C. Faul, J. Reiser, and P. Mundel Synaptopodin regulates the actin-bundling activity of alpha-actinin in an isoform-specific manner J Clin Invest 115 2005 1188 1198
42. S. Sever, M.M. Altintas, S.R. Nankoe, C.C. Moller, D. Ko, C. Wei, J. Henderson, E.C. del Re, L. Hsing, A. Erickson, C.D. Cohen, M. Kretzler, D. Kerjaschki, A. Rudensky, B. Nikolic, and J. Reiser Proteolytic processing of dynamin by cytoplasmic cathepsin L is a mechanism for proteinuric kidney disease J Clin Invest 117 2007 2095 2104
43. J. Reiser, B. Adair, and T. Reinheckel Specialized roles for cysteine cathepsins in health and disease J Clin Invest 120 2010 3421 3431
44. M. Blich, A. Golan, G. Arvatz, A. Sebbag, I. Shafat, E. Sabo, V. Cohen-Kaplan, S. Petcherski, S. Avniel-Polak, A. Eitan, H. Hammerman, D. Aronson, E. Axelman, N. Ilan, G. Nussbaum, and I. Vlodavsky Macrophage activation by heparanase is mediated by TLR-2 and TLR-4 and associates with plaque progression Arterioscler Thromb Vasc Biol 33 2013 e56 e65
45. G.J. Brunn, M.K. Bungum, G.B. Johnson, and J.L. Platt Conditional signaling by Toll-like receptor 4 FASEB J 19 2005 872 874
46. K.J. Goodall, I.K. Poon, S. Phipps, and M.D. Hulett Soluble heparan sulfate fragments generated by heparanase trigger the release of pro-inflammatory cytokines through TLR-4 PLoS One 9 2014 e109596
47. J.D. Ren, L. Fan, F.Z. Tian, K.H. Fan, B.T. Yu, W.H. Jin, Y.H. Tan, and L. Cheng Involvement of a membrane potassium channel in heparan sulphate-induced activation of macrophages Immunology 141 2014 345 352
48. H. Akbarshahi, J.B. Axelsson, K. Said, A. Malmstrom, H. Fischer, and R. Andersson TLR4 dependent heparan sulphate-induced pancreatic inflammatory response is IRF3-mediated J Transl Med 9 2011 219
49. L. Yu, L. Wang, and S. Chen Endogenous toll-like receptor ligands and their biological significance J Cell Mol Med 14 2010 2592 2603
50. G.B. Johnson, G.J. Brunn, Y. Kodaira, and J.L. Platt Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4 J Immunol 168 2002 5233 5239
51. D.L. Coleman, A.H. Bartiss, V.P. Sukhatme, J. Liu, and H.D. Rupprecht Lipopolysaccharide induces Egr-1 mRNA and protein in murine peritoneal macrophages J Immunol 149 1992 3045 3051