Full-length soluble urokinase plasminogen activator receptor down-modulates nephrin expression in podocytes

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Alfano, Massimo ^a   Cinque, Paola ^a   Giusti, Guido ^b   Proietti, Silvia ^b   Nebuloni, Manuela ^c   Danese, Silvio ^b   D'Alessio, Silvia ^b   Genua, Marco ^b   Portale, Federica ^b   Lo Porto, Manuela ^b   Singhal, Pravin C ^d   Rastaldi, Maria Pia ^e   Saleem, Moin A ^f   Mavilio, Domenico ^b,g   Mikulak, Joanna ^b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^e FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^f UNIVERSITY OF BRISTOL   (United Kingdom)

^g UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; NEPHRIN; PROTEIN BINDING; UROKINASE RECEPTOR; VITRONECTIN RECEPTOR; WT1 PROTEIN;

ANIMAL; BLOOD; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; MOUSE; PODOCYTE; PROMOTER REGION; PROTEINURIA;

ANIMALS; DOWN-REGULATION; GENE EXPRESSION REGULATION; GENETIC VARIATION; HUMANS; INTEGRIN ALPHAVBETA3; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PODOCYTES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEINURIA; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; WT1 PROTEINS;

EID: 84942049947     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13647     Document Type: Article

References (63)

1. Sidenius, N., Sier, C. F. & Blasi, F. Shedding and cleavage of the urokinase receptor (uPAR): identification and characterisation of uPAR fragments in vitro and in vivo. FEBS Lett 475, 52-56 (2000).
2. Thuno, M., Macho, B. & Eugen-Olsen, J. suPAR: the molecular crystal ball. Dis Markers 27, 157-172 (2009).
3. Eden, G., Archinti, M., Furlan, F., Murphy, R. & Degryse, B. The urokinase receptor interactome. Curr Pharm Des 17, 1874-1889 (2011).
4. Selleri, C. et al. Involvement of the urokinase-type plasminogen activator receptor in hematopoietic stem cell mobilization. Blood 105, 2198-2205 (2005).
5. Montuori, N. & Ragno, P. Multiple activities of a multifaceted receptor: roles of cleaved and soluble uPAR. Front Biosci (Landmark Ed) 14, 2494-2503 (2009).
6. Nebuloni, M. et al. HIV-1 infected lymphoid organs upregulate expression and release of the cleaved form of uPAR that modulates chemotaxis and virus expression. PLoS One 8, e70606 (2013).
7. Hoyer-Hansen, G., Behrendt, N., Ploug, M., Dano, K. & Preissner, K. T. The intact urokinase receptor is required for efficient vitronectin binding: receptor cleavage prevents ligand interaction. FEBS Lett 420, 79-85 (1997).
8. Wei, C. et al. Circulating urokinase receptor as a cause of focal segmental glomerulosclerosis. Nat Med 17, 952-960 (2011).
9. Meijers, B. et al. The soluble urokinase receptor is not a clinical marker for focal segmental glomerulosclerosis. Kidney Int 85, 636-640 (2014).
10. Wada, T. et al. A multicenter cross-sectional study of circulating soluble urokinase receptor in Japanese patients with glomerular disease. Kidney Int 85, 641-648 (2014).
11. Sinha, A. et al. Serum-soluble urokinase receptor levels do not distinguish focal segmental glomerulosclerosis from other causes of nephrotic syndrome in children. Kidney Int 85, 649-658 (2014).
12. Huang, J. et al. Plasma soluble urokinase receptor levels are increased but do not distinguish primary from secondary focal segmental glomerulosclerosis. Kidney Int 84, 366-372 (2013).
13. Bock, M. E., Price, H. E., Gallon, L. & Langman, C. B. Serum soluble urokinase-type plasminogen activator receptor levels and idiopathic FSGS in children: a single-center report. Clin J Am Soc Nephrol 8, 1304-1311 (2013).
14. Sidenius, N. et al. Serum level of soluble urokinase-type plasminogen activator receptor is a strong and independent predictor of survival in human immunodeficiency virus infection. Blood 96, 4091-4095 (2000).
15. Lomholt, A. F., Christensen, I. J., Hoyer-Hansen, G. & Nielsen, H. J. Prognostic value of intact and cleaved forms of the urokinase plasminogen activator receptor in a retrospective study of 518 colorectal cancer patients. Acta Oncol 49, 805-811 (2010).
16. Yilmaz, G., Koksal, I., Karahan, S. C. & Mentese, A. The diagnostic and prognostic significance of soluble urokinase plasminogen activator receptor in systemic inflammatory response syndrome. Clin Biochem 44, 1227-1230 (2011).
17. Mazar, A. P., Henkin, J. & Goldfarb, R. H. The urokinase plasminogen activator system in cancer: implications for tumor angiogenesis and metastasis. Angiogenesis 3, 15-32 (1999).
18. Cobos, E., Jumper, C. & Lox, C. Pretreatment determination of the serum urokinase plasminogen activator and its soluble receptor in advanced small-cell lung cancer or non-small-cell lung cancer. Clin Appl Thromb Hemost 9, 241-246 (2003).
19. Giamarellos-Bourboulis, E. J. et al. Risk assessment in sepsis: a new prognostication rule by APACHE II score and serum soluble urokinase plasminogen activator receptor. Crit Care 16, R149 (2012).
20. Zimmermann, H. W., Koch, A., Seidler, S., Trautwein, C. & Tacke, F. Circulating soluble urokinase plasminogen activator is elevated in patients with chronic liver disease, discriminates stage and aetiology of cirrhosis and predicts prognosis. Liver Int 32, 500-509 (2012).
21. Edsfeldt, A. et al. Soluble urokinase plasminogen activator receptor is associated with inflammation in the vulnerable human atherosclerotic plaque. Stroke 43, 3305-3312 (2012).
22. Kestila, M. et al. Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1, 575-582 (1998).
23. Lenkkeri, U. et al. Structure of the gene for congenital nephrotic syndrome of the finnish type (NPHS1) and characterization of mutations. Am J Hum Genet 64, 51-61 (1999).
24. Pollak, M. R. The genetic basis of FSGS and steroid-resistant nephrosis. Semin Nephrol 23, 141-146 (2003).
25. Topham, P. S. et al. Nephritogenic mAb 5-1-6 is directed at the extracellular domain of rat nephrin. J Clin Invest 104, 1559-1566 (1999).
26. Kawachi, H. et al. Cloning of rat nephrin: expression in developing glomeruli and in proteinuric states. Kidney Int 57, 1949-1961 (2000).
27. Luimula, P. et al. Nephrin in experimental glomerular disease. Kidney Int 58, 1461-1468 (2000).
28. Mathew, S., Chen, X., Pozzi, A. & Zent, R. Integrins in renal development. Pediatr Nephrol 27, 891-900 (2012).
29. Pozzi, A. & Zent, R. Integrins in kidney disease. J Am Soc Nephrol 24, 1034-1039 (2013).
30. Borza, C. M. et al. Human podocytes adhere to the KRGDS motif of the alpha3alpha4alpha5 collagen IV network. J Am Soc Nephrol 19, 677-684 (2008).
31. Reiser, J., Wei, C. & Tumlin, J. Soluble urokinase receptor and focal segmental glomerulosclerosis. Curr Opin Nephrol Hypertens 21, 428-432 (2012).
32. Reiser, J. & Sever, S. Podocyte biology and pathogenesis of kidney disease. Annu Rev Med 64, 357-366 (2013).
33. Wei, C. et al. Modification of kidney barrier function by the urokinase receptor. Nat Med 14, 55-63 (2008).
34. Saleem, M. A. et al. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol 13, 630-638 (2002).
35. Roldan, A. L. et al. Cloning and expression of the receptor for human urokinase plasminogen activator, a central molecule in cell surface, plasmin dependent proteolysis. EMBO J 9, 467-474 (1990).
36. Suzuki, A. et al. Retinoids regulate the repairing process of the podocytes in puromycin aminonucleoside-induced nephrotic rats. J Am Soc Nephrol 14, 981-991 (2003).
37. Wagner, N., Wagner, K. D., Xing, Y., Scholz, H. & Schedl, A. The major podocyte protein nephrin is transcriptionally activated by the Wilms' tumor suppressor WT1. J Am Soc Nephrol 15, 3044-3051 (2004).
38. Matsui, I. et al. Snail, a transcriptional regulator, represses nephrin expression in glomerular epithelial cells of nephrotic rats. Lab Invest 87, 273-283 (2007).
39. Moore, A. W. et al. YAC transgenic analysis reveals Wilms' tumour 1 gene activity in the proliferating coelomic epithelium, developing diaphragm and limb. Mech Dev 79, 169-184 (1998).
40. Kreidberg, J. A. et al. WT-1 is required for early kidney development. Cell 74, 679-691 (1993).
41. Davies, J. A. et al. Development of an siRNA-based method for repressing specific genes in renal organ culture and its use to show that the Wt1 tumour suppressor is required for nephron differentiation. Hum Mol Genet 13, 235-246 (2004).
42. Guo, J. K. et al. WT1 is a key regulator of podocyte function: reduced expression levels cause crescentic glomerulonephritis and mesangial sclerosis. Hum Mol Genet 11, 651-659 (2002).
43. Guo, G., Morrison, D. J., Licht, J. D. & Quaggin, S. E. WT1 activates a glomerular-specific enhancer identified from the human nephrin gene. J Am Soc Nephrol 15, 2851-2856 (2004).
44. Furuhata, A. et al. GATA-1 and GATA-2 binding to 3′ enhancer of WT1 gene is essential for its transcription in acute leukemia and solid tumor cell lines. Leukemia 23, 1270-1277 (2009).
45. Bourkoula, K. et al. The Wilms' tumor suppressor WT1 enhances CD95L expression and promotes activation-induced cell death in leukemic T cells. Int J Cancer 134, 291-300 (2014).
46. Outinen, T. K. et al. Urine soluble urokinase-type plasminogen activator receptor levels correlate with proteinuria in Puumala hantavirus infection. J Intern Med 276, 387-395 (2014).
47. Theilade, S. et al. Soluble urokinase plasminogen activator receptor levels are elevated and associated with complications in patients with type 1 diabetes. J Intern Med 277, 362-371 (2014).
48. Meijers, B. et al. Soluble urokinase receptor is a biomarker of cardiovascular disease in chronic kidney disease. Kidney Int 87, 210-216 (2014).
49. Mocroft, A. et al. Estimated glomerular filtration rate, chronic kidney disease and antiretroviral drug use in HIV-positive patients. AIDS 24, 1667-1678 (2010).
50. Mocroft, A. et al. Chronic renal failure among HIV-1-infected patients. AIDS 21, 1119-1127 (2007).
51. Ross, M. J. Advances in the pathogenesis of HIV-associated kidney diseases. Kidney Int 86, 266-274 (2014).
52. Maggi, P. et al. Renal complications in HIV disease: between present and future. AIDS Rev 14, 37-53 (2012).
53. Cathelin, D. et al. Administration of Recombinant Soluble Urokinase Receptor Per Se Is Not Sufficient to Induce Podocyte Alterations and Proteinuria in Mice. J Am Soc Nephrol 25, 1662-1668 (2014).
54. Jin, D. K. et al. Distribution of integrin subunits in human diabetic kidneys. J Am Soc Nephrol 7, 2636-2645 (1996).
55. Boettiger, D. et al. Regulation of integrin alpha 5 beta 1 affinity during myogenic differentiation. Dev Biol 169, 261-272 (1995).
56. Bitzan, M., Babayeva, S., Vasudevan, A., Goodyer, P. & Torban, E. TNFalpha pathway blockade ameliorates toxic effects of FSGS plasma on podocyte cytoskeleton and beta3 integrin activation. Pediatr Nephrol 27, 2217-2226 (2012).
57. Wei, C., Li, W. & Reiser, J. A common B3 integrin polymorphism L33P renders enhanced reactivity to soluble urokinase receptor: relevance to focal segmental glomerulosclerosis. Kideny Week 2013. Atlanta (GA): J Am Soc Nephrol 24, 571A (2013).
58. Andersen, O., Eugen-Olsen, J., Kofoed, K., Iversen, J. & Haugaard, S. B. suPAR associates to glucose metabolic aberration during glucose stimulation in HIV-infected patients on HAART. J Infect 57, 55-63 (2008).
59. Andersen, O., Eugen-Olsen, J., Kofoed, K., Iversen, J. & Haugaard, S. B. Soluble urokinase plasminogen activator receptor is a marker of dysmetabolism in HIV-infected patients receiving highly active antiretroviral therapy. J Med Virol 80, 209-216 (2008).
60. Ostrowski, S. R. et al. Plasma levels of intact and cleaved urokinase receptor decrease in HIV-1-infected patients initiating highly active antiretroviral therapy. Scand J Immunol 63, 478-486 (2006).
61. Alfano, M., Sidenius, N., Panzeri, B., Blasi, F. & Poli, G. Urokinase-urokinase receptor interaction mediates an inhibitory signal for HIV-1 replication. Proc Natl Acad Sci USA 99, 8862-8867 (2002).
62. Fazioli, F. et al. A urokinase-sensitive region of the human urokinase receptor is responsible for its chemotactic activity. Embo J 16, 7279-7286. (1997).
63. Dewerchin, M. et al. Generation and characterization of urokinase receptor-deficient mice. J Clin Invest 97, 870-878 (1996).