Impact of heparanase on renal fibrosis

Journal of Translational Medicine

Volumn 13, Issue 1, 2015, Pages

  Masola, Valentina ^a   Zaza, Gianluigi ^a   Onisto, Maurizio ^b   Lupo, Antonio ^a   Gambaro, Giovanni ^c  

^a UNIVERSITY HOSPITAL OF VERONA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BETA GLUCURONIDASE; BIOLOGICAL MARKER; FIBROBLAST GROWTH FACTOR 2; GLUCOSE; HEPARANASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SYNDECAN 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; HEPARANASE;

ALBUMINURIA; ARTICLE; DRUG TARGETING; ENZYME BLOOD LEVEL; EPITHELIAL MESENCHYMAL TRANSITION; GLUCOSE BLOOD LEVEL; HUMAN; KIDNEY FIBROSIS; KIDNEY TUBULE CELL; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; ENZYMOLOGY; FIBROSIS; KIDNEY; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY;

BIOMARKERS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROSIS; GLUCURONIDASE; HUMANS; KIDNEY; MOLECULAR TARGETED THERAPY;

EID: 84930674520     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-015-0538-5     Document Type: Article

References (57)

1. Friedman SL, Sheppard D, Duffield JS, Violette S (2013) Therapy for fibrotic diseases: nearing the starting line. Sci Transl Med 5:167sr1
2. US Renal Data System, USRDS (2013) Annual data report: atlas of chronic kidney disease and end-stage renal Disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda
3. Gambaro G, Yabarek T, Graziani MS, Gemelli A, Abaterusso C, Frigo AC et al; INCIPE Study Group (2010) Prevalence of CKD in northeastern Italy: results of the INCIPE study and comparison with NHANES. Clin J Am Soc Nephrol 5:1946-1953
4. Hewitson TD (2009) Renal tubulointerstitial fibrosis: common but never simple. Am J Physiol Renal Physiol 296:F1239-F1244
5. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY (2004) Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351:1296-1305
6. Duffield JS (2014) Cellular and molecular mechanisms in kidney fibrosis. J Clin Invest 124:2299-2306
7. Szymczak M, Kuźniar J, Klinger M (2010) The role of heparanase in diseases of the glomeruli. Arch Immunol Ther Exp (Warsz) 58:45-56
8. Ilan N, Elkin M, Vlodavsky I (2006) Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol 38:2018-2039
9. Bosman FT, Stamenkovic I (2003) Functional structure and composition of the extracellular matrix. J Pathol 200:423-428
10. Genovese F, Manresa AA, Leeming DJ, Karsdal MA, Boor P (2014) The extracellular matrix in the kidney: a source of novel non-invasive biomarkers of kidney fibrosis? Fibrogenesis Tissue Repair 7:4
11. Liu Y (2006) Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 69:213-217
12. LeBleu VS, Taduri G, O'Connell J, Teng Y, Cooke VG, Woda C et al (2013) Origin and function of myofibroblasts in kidney fibrosis. Nat Med 19:1047-1053
13. Lan HY (2003) Tubular epithelial-myofibroblast transdifferentiation mechanisms in proximal tubule cells. Curr Opin Nephrol Hypertens 12:25-29
14. Kanasaki K, Taduri G, Koya D (2013) Diabetic nephropathy: the role of inflammation in fibroblast activation and kidney fibrosis. Front Endocrinol (Lausanne) 4:7
15. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, du Bois RM (2005) Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 166:1321-1332
16. Hills CE, Squires PE (2010) TGF-beta1-induced epithelial-to-mesenchymal transition and therapeutic intervention in diabetic nephropathy. Am J Nephrol 31:68-74
17. Lee JM, Dedhar S, Kalluri R, Thompson EW (2006) The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 172:973-981
18. Carew RM, Wang B, Kantharidis P (2012) The role of EMT in renal fibrosis. Cell Tissue Res 347:103-116
19. Vreys V, David G (2007) Mammalian heparanase: what is the message? J Cell Mol Med 11:427-452
20. Vlodavsky I, Ilan N, Naggi A, Casu B (2007) Heparanase: structure, biological functions, and inhibition by heparin-derived mimetics of heparan sulfate. Curr Pharm Des 13:2057-2073
21. Vreys V, Delande N, Zhang Z, Coomans C, Roebroek A, Dürr J et al (2005) Cellular uptake of mammalian heparanase precursor involves low-density lipoprotein receptor-related proteins, mannose 6-phosphate receptors, and heparan sulfate proteoglycans. J Biol Chem 280:33141-33148
22. Fux L, Ilan N, Sanderson RD, Vlodavsky I (2009) Heparanase: busy at the cell surface. Trends Biochem Sci 34:511-519
23. Masola V, Gambaro G, Tibaldi E, Brunati AM, Gastaldello A, D'Angelo A et al (2012) Heparanase and syndecan-1 interplay orchestrates fibroblast growth factor-2-induced epithelial-mesenchymal transition in renal tubular cells. J Biol Chem 287:1478-1488
24. Masola V, Zaza G, Secchi MF, Gambaro G, Lupo A, Onisto M (2014) Heparanase is a key player in renal fibrosis by regulating TGF-β expression and activity. Biochim Biophys Acta 1843:2122-2128
25. Kato M, Wang H, Kainulainen V, Fitzgerald ML, Ledbetter S, Ornitz DM et al (1998) Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 4:691-697
26. Li JP, Vlodavsky I (2009) Heparin, heparan sulfate and heparanase in inflammatory reactions. Thromb Haemost 102:823-828
27. van den Hoven MJ, Rops AL, Vlodavsky I, Levidiotis V, Berden JH, van der Vlag J (2007) Heparanase in glomerular diseases. Kidney Int 72:543-548
28. Kramer A, van den Hoven M, Rops A, Wijnhoven T, van den Heuvel L, Lensen J et al (2006) Induction of glomerular heparanase expression in rats with adriamycin nephropathy is regulated by reactive oxygen species and the renin-angiotensin system. J Am Soc Nephrol 17:2513-2520
29. Garsen M, Rops AL, Rabelink TJ, Berden JH, van der Vlag J (2014) The role of heparanase and the endothelial glycocalyx in the development of proteinuria. Nephrol Dial Transpl 29:49-55
30. van den Hoven MJ, Rops AL, Bakker MA, Aten J, Rutjes N, Roestenberg P et al (2006) Increased expression of heparanase in overt diabetic nephropathy. Kidney Int 70:2100-2118
31. Masola V, Gambaro G, Tibaldi E, Onisto M, Abaterusso C, Lupo A (2011) Regulation of heparanase by albumin and advanced glycation end products in proximal tubular cells. Biochim Biophys Acta 1813:1475-1482
32. Gil N, Goldberg R, Neuman T, Garsen M, Zcharia E, Rubinstein AM et al (2012) Heparanase is essential for the development of diabetic nephropathy in mice. Diabetes 61:208-216
33. Lan A, Du J (2014) Potential role of Akt signaling in chronic kidney disease. Nephrol Dial Transpl (Epub ahead of print)
34. Loeffler I, Wolf G (2014) Transforming growth factor-β and the progression of renal disease. Nephrol Dial Transplant 29(Suppl 1):i37-i45
35. You H, Gao T, Cooper TK, Brian Reeves W, Awad AS (2013) Macrophages directly mediate diabetic renal injury. Am J Physiol Renal Physiol 305:F1719-F1727
36. Lerner I, Zcharia E, Neuman T, Hermano E, Rubinstein AM, Vlodavsky I et al (2014) Heparanase is preferentially expressed in human psoriatic lesions and induces development of psoriasiform skin inflammation in mice. Cell Mol Life Sci 71:2347-2357
37. Lerner I, Hermano E, Zcharia E, Rodkin D, Bulvik R, Doviner V et al (2011) Heparanase powers a chronic inflammatory circuit that promotes colitis-associated tumorigenesis in mice. J Clin Invest 121:1709-1721
38. Goldberg L, Rubinstein AM, Gil N, Hermano E, Li JP, van der Vlag J et al (2014) Role of heparanase-driven cascade in pathogenesis of diabetic nephropathy. Diabetes 63:4302-4313
39. Masola V, Maran C, Tassone E, Zin A, Rosolen A, Onisto M (2009) Heparanase activity in alveolar and embryonal rhabdomyosarcoma: implications for tumor invasion. BMC Cancer 9:304
40. Shafat I, Barak AB, Postovsky S, Elhasid R, Ilan N, Vlodavsky I et al (2007) Heparanase levels are elevated in the plasma of pediatric cancer patients and correlate with response to anticancer treatment. Neoplasia 9:909-916
41. Ben Arush MW, Shafat I, Ben Barak A, Shalom RB, Vlodavsky I, Ilan N (2009) Plasma heparanase as a significant marker of treatment response in children with Hodgkin lymphoma: pilot study. Pediatr Hematol Oncol 26:157-164
42. Shafat I, Ilan N, Zoabi S, Vlodavsky I, Nakhoul F (2011) Heparanase levels are elevated in the urine and plasma of type 2 diabetes patients and associate with blood glucose levels. PLoS One 6:e17312
43. Rops AL, van den Hoven MJ, Veldman BA, Salemink S, Vervoort G, Elving LD et al (2012) Urinary heparanase activity in patients with Type 1 and Type 2 diabetes. Nephrol Dial Transpl 27:2853-2861
44. Masola V, Zaza G, Onisto M, Lupo A, Gambaro G (2014) Glycosaminoglycans, proteoglycans and sulodexide and the endothelium: biological roles and pharmacological effects. Int Angiol 33:243-254
45. Shafat I, Agbaria A, Boaz M, Schwartz D, Baruch R, Nakash R et al (2012) Elevated urine heparanase levels are associated with proteinuria and decreased renal allograft function. PLoS One 7:e44076
46. Cohen-Mazor M, Sela S, Mazor R, Ilan N, Vlodavsky I, Rops AL et al (2008) Are primed polymorphonuclear leukocytes contributors to the high heparanase levels in hemodialysis patients? Am J Physiol Heart Circ Physiol 294:H651-H658
47. Zaza G, Masola V, Granata S, Pontrelli P, Sallustio F, Gesualdo L et al (2014) Dialysis-related transcriptomic profiling: the pivotal role of heparanase. Exp Biol Med (Maywood) 239:52-64
48. Masola V, Secchi MF, Gambaro G, Onisto M (2014) Heparanase as a target in cancer therapy. Curr Cancer Drug Targets 14:286-293
49. Naggi A, Casu B, Perez M, Torri G, Cassinelli G, Penco S et al (2005) Modulation of the heparanase-inhibiting activity of heparin through selective desulfation, graded N-acetylation, and glycol splitting. J Biol Chem 280:12103-12113
50. Liu CJ, Chang J, Lee PH, Lin DY, Wu CC, Jeng LB et al (2014) Adjuvant heparanase inhibitor PI-88 therapy for hepatocellular carcinoma recurrence. World J Gastroenterol 20:11384-11393
51. Masola V, Onisto M, Zaza G, Lupo A, Gambaro G (2012) A new mechanism of action of sulodexide in diabetic nephropathy: inhibits heparanase-1 and prevents FGF-2-induced renal epithelial-mesenchymal transition. J Transl Med 10:213
52. Masola V, Zaza G, Gambaro G (2014) Sulodexide and glycosaminoglycans in the progression of renal disease. Nephrol Dial Transpl 29(Suppl 1):i74-i79
53. Ceol M, Gambaro G, Sauer U, Baggio B, Anglani F, Forino M et al (2000) Glycosaminoglycan therapy prevents TGF-beta1 overexpression and pathologic changes in renal tissue of long-term diabetic rats. J Am Soc Nephrol 11:2324-2336
54. Yung S, Chau MK, Zhang Q, Zhang CZ, Chan TM (2013) Sulodexide decreases albuminuria and regulates matrix protein accumulation in C57BL/6 mice with streptozotocin-induced type I diabetic nephropathy. PLoS One 8:e54501
55. Afsar B, Turkmen K, Covic A, Kanbay M (2014) An update on coronary artery disease and chronic kidney disease. Int J Nephrol 2014:767424
56. Coccheri S, Scondotto G, Agnelli G, Palazzini E, Zamboni V; Arterial Arm of the Suavis (Sulodexide Arterial Venous Italian Study) group (2002) Sulodexide in the treatment of intermittent claudication. Results of a randomized, double-blind, multicentre, placebo-controlled study. Eur Heart J 23:1057-1065
57. Condorelli M, Chiariello M, Dagianti A, Penco M, Dalla Volta S, Pengo V et al (1994) IPO-V2: a prospective, multicenter, randomized, comparative clinical investigation of the effects of sulodexide in preventing cardiovascular accidents in the first year after acute myocardial infarction. J Am Coll Cardiol 23:27-34