Heparanase and syndecan-1 interplay orchestrates fibroblast growth factor-2-induced epithelial-mesenchymal transition in renal tubular cells

Journal of Biological Chemistry

Volumn 287, Issue 2, 2012, Pages 1478-1488

  Masola, Valentina ^a   Gambaro, Giovanni ^c   Tibaldi, Elena ^a   Brunati, Anna Maria ^a   Gastaldello, Alessandra ^a   D'Angelo, Angela ^a   Onisto, Maurizio ^a   Lupo, Antonio ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOCRINE LOOP; END STAGE RENAL DISEASE; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLAST GROWTH; HEPARAN SULFATES; HEPARANASE; HUMAN KIDNEY; INTRACELLULAR SIGNALING; MATRIX METALLOPROTEINASE-9; MYOFIBROBLASTS; RENAL FIBROSIS; SYNDECAN-1; TUBULAR CELLS; WILD TYPES;

CLONE CELLS; ENZYME ACTIVITY; FIBROBLASTS; GROWTH KINETICS;

CELL CULTURE;

GELATINASE B; HEPARANASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SYNDECAN 1;

ARTICLE; AUTOCRINE EFFECT; CELL CLONE; CELL CULTURE; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME STABILITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; KIDNEY TUBULE CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

AUTOCRINE COMMUNICATION; CELL LINE; ENZYME ACTIVATION; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLAST GROWTH FACTOR 2; FIBROSIS; GLUCURONIDASE; HUMANS; KIDNEY FAILURE, CHRONIC; KIDNEY TUBULES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; SYNDECAN-1;

EID: 84855489306     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.279836     Document Type: Article

References (36)

1. Hewitson, T. D. (2009) Renal tubulointerstitial fibrosis: common but never simple. Am. J. Physiol. Renal Physiol. 296, F1239-44
2. Nath, K. A. (1998) The tubulointerstitium in progressive renal disease. Kidney Int. 54, 992-994
3. Iwano, M., Plieth, D., Danoff, T. M., Xue, C., Okada, H., and Neilson, E. G. (2002) Evidence that fibroblasts derive from epithelium during tissue fibrosis. J. Clin. Invest. 110, 341-350 (Pubitemid 34847966)
4. Liu, Y. (2010) New insights into epithelial-mesenchymal transition in kidney fibrosis. J. Am. Soc. Nephrol. 21, 212-222
5. Strutz, F. M. (2009) EMT and proteinuria as progression factors. Kidney Int. 75, 475-481
6. Lan, H. Y. (2003) Tubular epithelial-myofibroblast transdifferentiation mechanisms in proximal tubule cells. Curr. Opin. Nephrol. Hypertens. 12, 25-29
7. Burns, W. C., Twigg, S. M., Forbes, J. M., Pete, J., Tikellis, C., Thallas- Bonke, V., Thomas, M. C., Cooper, M. E., and Kantharidis, P. (2006) Connective tissue growth factor plays an important role in advanced glycation end product-induced tubular epithelial-to-mesenchymal transition: implications for diabetic renal disease. J. Am. Soc. Nephrol. 17, 2484-2494 (Pubitemid 44300964)
8. Ha, H., and Lee, H. B. (2003) Reactive oxygen species and matrix remodeling in diabetic kidney. J. Am. Soc. Nephrol. 14, S246-249 (Pubitemid 36903934)
9. Strutz, F., Zeisberg, M., Ziyadeh, F. N., Yang, C. Q., Kalluri, R., Müller, G. A., and Neilson, E. G. (2002) Role of basic fibroblast growth factor-2 in epithelial-mesenchymal transformation. Kidney Int. 61, 1714-1728 (Pubitemid 34437925)
10. Schlessinger, J. (2000) Cell signaling by receptor tyrosine kinases. Cell 103, 211-225
11. Dailey, L., Ambrosetti, D., Mansukhani, A., and Basilico, C. (2005) Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev. 16, 233-247 (Pubitemid 40616120)
12. Katoh, M., and Katoh, M. (2006) Cross-talk of WNT and FGF signaling pathways at GSK3β to regulate β-catenin and SNAIL signaling cascades. Cancer Biol. Ther. 5, 1059-1064 (Pubitemid 44772212)
13. Kato, M., Saunders, S., Nguyen, H., and Bernfield, M. (1995) Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells. Mol. Biol. Cell 6, 559-576
14. Mali, M., Elenius, K., Miettinen, H. M., and Jalkanen, M. (1993) Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1. J. Biol. Chem. 268, 24215-24222 (Pubitemid 23335407)
15. Kato, M., Wang, H., Kainulainen, V., Fitzgerald, M. L., Ledbetter, S., Ornitz, D. M., and Bernfield, M. (1998) Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat. Med. 4, 691-697 (Pubitemid 28274669)
16. Ilan, N., Elkin, M., and Vlodavsky, I. (2006) Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int. J. Biochem. Cell Biol. 38, 2018-2039 (Pubitemid 44397619)
17. Purushothaman, A., Hurst, D. R., Pisano, C., Mizumoto, S., Sugahara, K., and Sanderson, R. D. (2011) Heparanase-mediated loss of nuclear syndecan- 1 enhances histone acetyltransferase (HAT) activity to promote expression of genes that drive an aggressive tumor phenotype. J. Biol. Chem. 286, 30377-30383
18. Fux, L., Ilan, N., Sanderson, R. D., and Vlodavsky, I. (2009) Heparanase: busy at the cell surface. Trends Biochem. Sci. 34, 511-519
19. Zong, F., Fthenou, E., Wolmer, N., Hollósi, P., Kovalszky, I., Szilák, L., Mogler, C., Nilsonne, G., Tzanakakis, G., and Dobra, K. (2009) Syndecan-1 and FGF-2, but not FGF receptor-1, share a common transport route and co-localize with heparanase in the nuclei of mesenchymal tumor cells. PLoS One 4, e7346
20. Reiland, J., Kempf, D., Roy, M., Denkins, Y., and Marchetti, D. (2006) FGF2 binding, signaling, and angiogenesis are modulated by heparanase in metastatic melanoma cells. Neoplasia 8, 596-606 (Pubitemid 44061315)
21. van den Hoven, M. J., Rops, A. L., Vlodavsky, I., Levidiotis, V., Berden, J. H., and van der Vlag, J. (2007) Heparanase in glomerular diseases. Kidney Int. 72, 543-548 (Pubitemid 47312787)
22. Masola, V., Gambaro, G., Tibaldi, E., Onisto, M., Abaterusso, C., and Lupo, A. (2011) Regulation of heparanase by albumin and advanced glycation end products in proximal tubular cells. Biochim. Biophys. Acta 1813, 1475-1482
23. Masola, V., Maran, C., Tassone, E., Zin, A., Rosolen, A., and Onisto, M. (2009) Heparanase activity in alveolar and embryonal rhabdomyosarcoma: implications for tumor invasion. BMC Cancer 9, 304
24. Onisto, M., Slongo, M. L., Gregnanin, L., Gastaldi, T., Carli, M., and Rosolen, A. (2005) Expression and activity of vascular endothelial growth factor and metalloproteinases in alveolar and embryonal rhabdomyosarcoma cell lines. Int. J. Oncol. 27, 791-798
25. Liang, C. C., Park, A. Y., and Guan, J. L. (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2, 329-333 (Pubitemid 47040047)
26. Almeida, S., Cunha-Oliveira, T., Laço, M., Oliveira, C. R., and Rego, A. C. (2010) Dysregulation of CREB activation and histone acetylation in 3-nitropropionic acid-treated cortical neurons: prevention by BDNF and NGF. Neurotox. Res. 17, 399-405
27. Steffes, M. W., Osterby, R., Chavers, B., and Mauer, S. M. (1989) Mesangial expansion as a central mechanism for loss of kidney function in diabetic patients. Diabetes 38, 1077-1081 (Pubitemid 19250390)
28. Gambaro, G., and Baggio, B. (1992) Role of glycosaminoglycans in diabetic nephropathy. Acta Diabetol. 29, 149-155
29. Morita, H., Shinzato, T., David, G., Mizutani, A., Habuchi, H., Fujita, Y., Ito, M., Asai, J., Maeda, K., and Kimata, K. (1994) Basic fibroblast growth factor-binding domain of heparan sulfate in the human glomerulosclerosis and renal tubulointerstitial fibrosis. Lab. Invest. 71, 528-535 (Pubitemid 24338160)
30. Ray, P. E., Bruggeman, L. A., Weeks, B. S., Kopp, J. B., Bryant, J. L., Owens, J. W., Notkins, A. L., and Klotman, P. E. (1994) bFGF and its low affinity receptors in the pathogenesis of HIV-associated nephropathy in trans- genic mice. Kidney Int. 46, 759-772 (Pubitemid 24272034)
31. Thiery, J. P., and Sleeman, J. P. (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142 (Pubitemid 43278296)
32. Rane,M.J., Song, Y., Jin, S., Barati,M.T.,Wu,R., Kausar, H., Tan, Y.,Wang,Y., Zhou, G., Klein, J. B., Li, X., and Cai, L. (2010) Interplay between Akt and p38 MAPK pathways in the regulation of renal tubular cell apoptosis associated with diabetic nephropathy. Am. J. Physiol. Renal Physiol. 298, F49-61
33. Brule, S., Charnaux, N., Sutton, A., Ledoux, D., Chaigneau, T., Saffar, L., and Gattegno, L. (2006) The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/ CXCL12 and mediated by the matrix metalloproteinase-9. Glycobiology 16, 488-501 (Pubitemid 43779045)
34. Sharma, K., Jin, Y., Guo, J., and Ziyadeh, F. N. (1996) Neutralization of TGF-β by anti-TGF-β antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 45, 522-530
35. Border, W. A., and Ruoslahti, E. (1992) Transforming growth factor-β in disease: the dark side of tissue repair. J. Clin. Invest. 90, 1-7
36. Szymczak, M., Kuzniar, J., and Klinger, M. (2010) The role of heparanase in diseases of the glomeruli. Arch. Immunol. Ther. Exp. 58, 45-56