Focal segmental glomerulosclerosis is induced by microRNA-193a and its downregulation of WT1

Nature Medicine

Volumn 19, Issue 4, 2013, Pages 481-487

  Gebeshuber, Christoph A ^a,b   Kornauth, Christoph ^a   Dong, Lihua ^c   Sierig, Ralph ^c   Seibler, Jost ^d   Reiss, Martina ^d   Tauber, Stefanie ^e   Bilban, Martin ^a   Wang, Shijun ^f   Kain, Renate ^a   Böhmig, Georg A ^a   Moeller, Marcus J ^g   Gröne, Hermann Josef ^f   Englert, Christoph ^c   Martinez, Javier ^b   Kerjaschki, Dontscho ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

^c FRITZ LIPMANN INSTITUTE   (Germany)

^d TaconicArtemis GmbH   (Germany)

^e UNIVERSITY OF VIENNA   (Austria)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 193A; NEPHRIN; PODOCALYXIN; TRANSCRIPTION FACTOR; TUMOR PROTEIN; UNCLASSIFIED DRUG; WILMS TUMOR PROTEIN 1; DOXYCYCLINE; MIRN193 MICRORNA, HUMAN; MIRN193 MICRORNA, MOUSE; WT1 PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; FOCAL GLOMERULOSCLEROSIS; GENE EXPRESSION; GENE TARGETING; GLOMERULOPATHY; HOMEOSTASIS; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; UPREGULATION; ANIMAL; GENETICS; KIDNEY; MALE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

MUS;

ANIMALS; DOWN-REGULATION; DOXYCYCLINE; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; KIDNEY; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICRORNAS; PODOCYTES; WT1 PROTEINS;

MLCS; MLOWN;

EID: 84878425125     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3142     Document Type: Article

References (51)

1. D'Agati, V.D., Kaskel, F.J. & Falk, R.J. Focal segmental glomerulosclerosis. N. Engl. J. Med. 365, 2398-2411 (2011).
2. Wiggins, R.C. The spectrum of podocytopathies: a unifying view of glomerular diseases. Kidney Int. 71, 1205-1214 (2007).
3. Inui, M., Martello, G. & Piccolo, S. MicroRNA control of signal transduction. Nat. Rev. Mol. Cell Biol. 11, 252-263 (2010).
4. Kato, M., Park, J.T. & Natarajan, R. MicroRNA and the glomerulus. Exp. Cell Res. 318, 993-1000 (2012).
5. Bennett, M.R. et al. Laser capture microdissection-microarray analysis of focal segmental glomerulosclerosis glomeruli. Nephron Exp. Nephrol. 107, e30-e40 (2007).
6. Hodgin, J.B. et al. A molecular profile of focal segmental glomerulosclerosis from formalin-fixed, paraffin-embedded tissue. Am. J. Pathol. 177, 1674-1686 (2010).
7. Shi, S. et al. Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J. Am. Soc. Nephrol. 19, 2159-2169 (2008).
8. Morrison, A.A., Viney, R.L., Saleem, M.A. & Ladomery, M.R. New insights into the function of the Wilm tumor suppressor gene WT1 in podocytes. Am. J. Physiol. Renal Physiol. 295, F12-F17 (2008).
9. Seibler, J. et al. Reversible gene knockdown in mice using a tight, inducible shRNA expression system. Nucleic Acids Res. 35, e54 (2007).
10. Takemoto, M. et al. A new method for large scale isolation of kidney glomeruli from mice. Am. J. Pathol. 161, 799-805 (2002).
11. Creighton, C.J., Nagaraja, A.K., Hanash, S.M., Matzuk, M.M. & Gunaratne, P.H. A bioinformatics tool for linking gene expression profiling results with public databases of microRNA target predictions. RNA 14, 2290-2296 (2008).
12. John, B., et al. Human MicroRNA targets. PLoS Biol. 2, e363 (2004).
13. Ohtaka, A., Ootaka, T., Sato, H. & Ito, S. Phenotypic change of glomerular podocytes in primary focal segmental glomerulosclerosis: developmental paradigm? Nephrol. Dial. Transplant. 17 (suppl. 9), 11-15 (2002).
14. Chau, Y.Y. et al. Acute multiple organ failure in adult mice deleted for the developmental regulator WT1. PLoS Genet. 7, e1002404 (2011).
15. Palmer, R.E. et al. WT1 regulates the expression of the major glomerular podocyte membrane protein Podocalyxin. Curr. Biol. 11, 1805-1809 (2001).
16. 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).
17. Ratelade, J. et al. A murine model of Denys-Drash syndrome reveals novel transcriptional targets of WT1 in podocytes. Hum. Mol. Genet. 19, 1-15 (2010).
18. Schumacher, V.A. et al. WT1-dependent sulfatase expression maintains the normal glomerular filtration barrier. J. Am. Soc. Nephrol. 22, 1286-1296 (2011).
19. Kreidberg, J.A. et al. WT-1 is required for early kidney development. Cell 74, 679-691 (1993).
20. Shigehara, T. et al. Inducible podocyte-specific gene expression in transgenic mice. J. Am. Soc. Nephrol. 14, 1998-2003 (2003).
21. Schönig, K., Schwenk, F., Rajewsky, K. & Bujard, H. Stringent doxycycline dependent control of CRE recombinase in vivo. Nucleic Acids Res. 30, e134 (2002).
22. Venkatachalam, M.A., Cotran, R.S. & Karnovsky, M.J. An ultrastructural study of glomerular permeability in aminonucleoside nephrosis using catalase as a tracer protein. J. Exp. Med. 132, 1168-1180 (1970).
23. Kaplan, B.S., Renaud, L. & Drummond, K.N. Effects of aminonucleoside, daunomycin, and adriamycin on carbon oxidation by glomeruli. Lab Invest. 34, 174-178 (1976).
24. Binder, C.J., Weiher, H., Exner, M. & Kerjaschki, D. Glomerular overproduction of oxygen radicals in Mpv17 gene-inactivated mice causes podocyte foot process flattening and proteinuria: a model of steroid-resistant nephrosis sensitive to radical scavenger therapy. Am. J. Pathol. 154, 1067-1075 (1999).
25. Wei, C. et al. Circulating urokinase receptor as a cause of focal segmental glomerulosclerosis. Nat. Med. 17, 952-960 (2011).
26. Farquhar, M.G., Saito, A., Kerjaschki, D. & Orlando, R.A. The Heymann nephritis antigenic complex: megalin (gp330) and RAP. J. Am. Soc. Nephrol. 6, 35-47 (1995).
27. Seiler, M.W., Venkatachalam, M.A. & Cotran, R.S. Glomerular epithelium: structural alterations induced by polycations. Science 189, 390-393 (1975).
28. Kashtan, C., Fish, A.J., Kleppel, M., Yoshioka, K. & Michael, A.F. Nephritogenic antigen determinants in epidermal and renal basement membranes of kindreds with Alport-type familial nephritis. J. Clin. Invest. 78, 1035-1044 (1986).
29. Juhila, J. et al. Inducible nephrin transgene expression in podocytes rescues nephrin-deficient mice from perinatal death. Am. J. Pathol. 176, 51-63 (2010).
30. Barisoni, L., Bruggeman, L.A., Mundel, P., D'Agati, V.D. & Klotman, P.E. HIV-1 induces renal epithelial dedifferentiation in a transgenic model of HIV-associated nephropathy. Kidney Int. 58, 173-181 (2000).
31. Alpers, C.E. & Hudkins, K.L. Mouse models of diabetic nephropathy. Curr. Opin. Nephrol. Hypertens. 20, 278-284 (2011).
32. Obad, S. et al. Silencing of microRNA families by seed-targeting tiny LNAs. Nat. Genet. 43, 371-378 (2011).
33. Zhdanova, O. et al. The inducible deletion of Drosha and microRNAs in mature podocytes results in a collapsing glomerulopathy. Kidney Int. 80, 719-730 (2011).
34. 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).
35. Ross, M.D. et al. Math6 expression during kidney development and altered expression in a mouse model of glomerulosclerosis. Dev. Dyn. 235, 3102-3109 (2006).
36. Kerjaschki, D., Sharkey, D.J. & Farquhar, M.G. Identification and characterization of podocalyxin-the major sialoprotein of the renal glomerulus. J. Cell Biol. 98, 1591-1596 (1984).
37. Takeda, T., McQuistan, T., Orlando, R.A. & Farquhar, M.G. Loss of glomerular foot processes is associated with uncoupling of podocalyxin from the actin cytoskeleton. J. Clin. Invest. 108, 289-301 (2001).
38. Doyonnas, R. et al. Anuria, omphalocele and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J. Exp. Med. 194, 13-27 (2001).
39. Huber, T.B. & Benzing, T. The slit diaphragm: a signalling platform to regulate podocyte function. Curr. Opin. Nephrol. Hypertens. 14, 211-216 (2005).
40. 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).
41. Rantanen, M. et al. Nephrin TRAP mice lack slit diaphragms and show fibrotic glomeruli and cystic tubular lesions. J. Am. Soc. Nephrol. 13, 1586-1594 (2002).
42. Greka, A. & Mundel, P. Cell biology and pathology of podocytes. Annu. Rev. Physiol. 74, 299-323 (2012).
43. Welsh, G.I. & Saleem, M.A. The podocyte cytoskeleton-key to a functioning glomerulus in health and disease. Nat. Rev. Nephrol. 8, 14-21 (2012).
44. Giannico, G., Yang, H., Neilson, E.G. & Fogo, A.B. Dystroglycan in the diagnosis of FSGS. Clin. J. Am. Soc. Nephrol. 4, 1747-1753 (2009).
45. Seibler, J. et al. Single copy shRNA configuration for ubiquitous gene knockdown in mice. Nucleic Acids Res. 33, e67 (2005).
46. Wang, S. et al. Recipient Toll-like receptors contribute to chronic graft dysfunction by both MyD88-and TRIF-dependent signaling. Dis. Model Mech. 3, 92-103 (2010).
47. Mundel, P., Reiser, J. & Kriz, W. Induction of differentiation in cultured rat and human podocytes. J. Am. Soc. Nephrol. 8, 697-705 (1997).
48. 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).
49. Grant, G.R. et al. Comparative analysis of RNA-Seq alignment algorithms and the RNA-Seq unified mapper (RUM). Bioinformatics 27, 2518-2528 (2011).
50. Kerjaschki, D. et al. Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat. Med. 12, 230-234 (2006).
51. Michael, A.F., Blau, E. & Vernier, R.L. Glomerular polyanion: alteration in aminonucleoside nephrosis. Lab. Invest. 23, 649-657 (1970).