Lyso-Gb3 activates Notch1 in human podocytes

Human Molecular Genetics

Volumn 24, Issue 20, 2015, Pages 5720-5732

  Sanchez Niño, Maria D ^a,b,c   Carpio, Daniel ^d   Sanz, Ana Belen ^a,b,c   Ruiz Ortega, Marta ^a,b,c   Mezzano, Sergio ^d   Ortiz, Alberto ^a,b,c  

^a UAM)   (Spain)

^b Instituto Reina Sofia de Investigacion Nefrol Ogica   (Spain)

^c REDINREN   (Spain)

^d UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; FIBRONECTIN; GAMMA SECRETASE INHIBITOR; GLYCOLIPID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JAGGED1; LYSO GB3; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NOTCH1 RECEPTOR; PARTHENOLIDE; RANTES; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CALCIUM BINDING PROTEIN; GLOBOTRIAOSYL LYSOSPHINGOLIPID; HES1 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MEMBRANE PROTEIN; NOTCH1 PROTEIN, HUMAN; SERRATE PROTEINS; SIGNAL PEPTIDE; SPHINGOLIPID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FABRY DISEASE; FEMALE; FIBROGENESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; KIDNEY BIOPSY; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENETICS; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; FABRY DISEASE; FEMALE; FIBRONECTINS; GLYCOLIPIDS; HOMEODOMAIN PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; PODOCYTES; RECEPTOR, NOTCH1; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; UP-REGULATION;

EID: 84943810808     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv291     Document Type: Article

References (57)

1. Germain, D.P. (2010) Fabry disease. Orphanet J. Rare Dis., 5, 30.
2. Askari, H., Kaneski, C.R., Semino-Mora, C., Desai, P., Ang, A., Kleiner, D.E., Perlee, L.T., Quezado, M., Spollen, L.E., Wustman, B.A. et al. (2007) Cellular and tissue localization of globotriaosylceramide in Fabry disease. Virchows Arch., 451, 823-834.
3. Torra, R. and Ortiz, A. (2012) Fabry disease: the many faces of a single disorder. Clin. Kidney J., 5, 379-382.
4. Ortiz, A., Oliveira, J.P.,Waldek, S.,Warnock, D.G., Cianciaruso, B. and Wanner, C. (2008) Nephropathy in males and females with Fabry disease: cross-sectional description of patients before treatment with enzyme replacement therapy. Nephrol. Dial. Transpl., 23, 1600-1607.
5. Weidemann, F., Sanchez-Nino, M.D., Politei, J., Oliveira, J.P., Wanner, C., Warnock, D.G. and Ortiz, A. (2013) Fibrosis: a key feature of Fabry disease with potential therapeutic implications. Orphanet J. Rare Dis., 8, 116.
6. Valbuena, C., Oliveira, J.P., Carneiro, F., Relvas, S., Ganhao, M., Sa-Miranda, M.C. and Rodrigues, L.G. (2011) Kidney histologic alterations in alpha-galactosidase-deficient mice. Virchows Arch., 458, 477-486.
7. Terryn,W., Cochat, P., Froissart, R., Ortiz, A., Pirson, Y., Poppe, B., Serra, A., Van, B.W., Vanholder, R. and Wanner, C. (2013) Fabry nephropathy: indications for screening and guidance for diagnosis and treatment by the European Renal Best Practice. Nephrol. Dial. Transpl., 28, 505-517.
8. Warnock, D.G., Ortiz, A., Mauer, M., Linthorst, G.E., Oliveira, J. P., Serra, A.L., Marodi, L., Mignani, R., Vujkovac, B., Beitner-Johnson, D. et al. (2012) Renal outcomes of agalsidase beta treatment for Fabry disease: role of proteinuria and timing of treatment initiation. Nephrol. Dial. Transpl., 27, 1042-1049.
9. Ortiz, A., Cianciaruso, B., Cizmarik, M., Germain, D.P., Mignani, R., Oliveira, J.P., Villalobos, J., Vujkovac, B., Waldek, S., Wanner, C. et al. (2010) End-stage renal disease in patients with Fabry disease: natural history data from the Fabry Registry. Nephrol. Dial. Transpl., 25, 769-775.
10. Germain, D.P., Waldek, S., Banikazemi, M., Bushinsky, D.A., Charrow, J., Desnick, R.J., Lee, P., Loew, T., Vedder, A.C., Abichandani, R. et al. (2007) Sustained, long-term renal stabilization after 54 months of agalsidase beta therapy in patients with Fabry disease. J. Am. Soc. Nephrol., 18, 1547-1557.
11. Fernandez-Fernandez, B., Ortiz, A., Gomez-Guerrero, C. and Egido, J. (2014) Therapeutic approaches to diabetic nephropathy- beyond the RAS. Nat. Rev. Nephrol., 10, 325-346.
12. Ortiz, A., Oliveira, J.P., Wanner, C., Brenner, B.M., Waldek, S. and Warnock, D.G. (2008) Recommendations and guidelines for the diagnosis and treatment of Fabry nephropathy in adults. Nat. Clin. Pract. Nephrol., 4, 327-336.
13. Tahir, H., Jackson, L.L. and Warnock, D.G. (2007) Antiproteinuric therapy and Fabry nephropathy: sustained reduction of proteinuria in patients receiving enzyme replacement therapy with agalsidase-beta. J. Am. Soc. Nephrol., 18, 2609-2617.
14. Sanchez-Nino, M.D., Sanz, A.B., Carrasco, S., Saleem, M.A., Mathieson, P.W., Valdivielso, J.M., Ruiz-Ortega, M., Egido, J. and Ortiz, A. (2011) Globotriaosylsphingosine actions on human glomerular podocytes: implications for Fabry nephropathy. Nephrol. Dial. Transpl., 26, 1797-1802.
15. Pisani, A., Sabbatini, M., Duro, G., Colomba, P. and Riccio, E. (2015) Antiproteinuric effect of add-on paricalcitol in Fabry disease patients: a prospective observational study. Nephrol. Dial. Transpl., 30, 661-666.
16. Najafian, B., Svarstad, E., Bostad, L., Gubler, M.C., Tondel, C., Whitley, C. and Mauer, M. (2011) Progressive podocyte injury and globotriaosylceramide (GL-3) accumulation in young patients with Fabry disease. Kidney Int., 79, 663-670.
17. Tondel, C., Bostad, L., Larsen, K.K., Hirth, A., Vikse, B.E., Houge, G. and Svarstad, E. (2013) Agalsidase benefits renal histology in young patients with Fabry disease. J. Am. Soc. Nephrol., 24, 137-148.
18. Tondel, C., Bostad, L., Hirth, A. and Svarstad, E. (2008) Renal biopsy findings in children and adolescents with Fabry disease and minimal albuminuria. Am. J. Kidney Dis., 51, 767-776.
19. Aerts, J.M., Groener, J.E., Kuiper, S., Donker-Koopman, W.E., Strijland, A., Ottenhoff, R., van, R.C., Mirzaian, M., Wijburg, F.A., Linthorst, G.E. et al. (2008) Elevated globotriaosylsphingosine is a hallmark of Fabry disease. Proc. Natl Acad. Sci. USA, 105, 2812-2817.
20. Wang, Y., Deb, D.K., Zhang, Z., Sun, T., Liu,W., Yoon, D., Kong, J., Chen, Y., Chang, A. and Li, Y.C. (2012) Vitamin D receptor signaling in podocytes protects against diabetic nephropathy. J. Am. Soc. Nephrol., 23, 1977-1986.
21. Sanchez-Nino, M.D., Benito-Martin, A. and Ortiz, A. (2010) Newparadigms in cell death in human diabetic nephropathy. Kidney Int., 78, 737-744.
22. Sanchez-Nino, M.D., Bozic, M., Cordoba-Lanus, E., Valcheva, P., Gracia, O., Ibarz, M., Fernandez, E., Navarro-Gonzalez, J.F., Ortiz, A. and Valdivielso, J.M. (2012) Beyond proteinuria: VDR activation reduces renal inflammation in experimental diabetic nephropathy. Am. J. Physiol. Renal Physiol., 302, F647-F657.
23. Sanchez-Nino, M.D. and Ortiz, A. (2012) Notch3 and kidney injury: never two without three. J. Pathol., 228, 266-273.
24. Sirin, Y. and Susztak, K. (2012) Notch in the kidney: development and disease. J. Pathol., 226, 394-403.
25. Niranjan, T., Bielesz, B., Gruenwald, A., Ponda, M.P., Kopp, J.B., Thomas, D.B. and Susztak, K. (2008) The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat. Med., 14, 290-298.
26. Bielesz, B., Sirin, Y., Si, H., Niranjan, T., Gruenwald, A., Ahn, S., Kato, H., Pullman, J., Gessler, M., Haase, V.H. and Susztak, K. (2010) Epithelial Notch signaling regulates interstitial fibrosis development in the kidneys of mice and humans. J. Clin. Invest., 120, 4040-4054.
27. Murea, M., Park, J.K., Sharma, S., Kato, H., Gruenwald, A., Niranjan, T., Si, H., Thomas, D.B., Pullman, J.M. and Melamed, M. L. et al. (2010) Expression of Notch pathway proteins correlates with albuminuria, glomerulosclerosis, and renal function. Kidney Int., 78, 514-522.
28. Waters, A.M., Wu, M.Y., Huang, Y.W., Liu, G.Y., Holmyard, D., Onay, T., Jones, N., Egan, S.E., Robinson, L.A. and Piscione, T.D. (2012) Notch promotes dynamin-dependent endocytosis of nephrin. J. Am. Soc. Nephrol., 23, 27-35.
29. Cigna, D., D'Anna, C., Zizzo, C., Francofonte, D., Sorrentino, I., Colomba, P., Albeggiani, G., Armini, A., Bianchi, L., Bini, L. et al. (2013) Alteration of proteomic profiles in PBMC isolated from patients with Fabry disease: preliminary findings. Mol. Biosyst., 9, 1162-1168.
30. De Francesco, P.N., Mucci, J.M., Ceci, R., Fossati, C.A. and Rozenfeld, P.A. (2013) Fabry disease peripheral blood immune cells release inflammatory cytokines: role of globotriaosylceramide. Mol. Genet. Metab., 109, 93-99.
31. Pereira, C.S., Azevedo, O., Maia, M.L., Dias, A.F., Sa-Miranda, C. and Macedo, M.F. (2013) Invariant natural killer T cells are phenotypically and functionally altered in Fabry disease. Mol. Genet. Metab., 108, 241-248.
32. Biancini, G.B., Vanzin, C.S., Rodrigues, D.B., Deon, M., Ribas, G. S., Barschak, A.G., Manfredini, V., Netto, C.B., Jardim, L.B., Giugliani, R. et al. (2012) Globotriaosylceramide is correlated with oxidative stress and inflammation in Fabry patients treated with enzyme replacement therapy. Biochim. Biophys. Acta, 1822, 226-232.
33. Kikumoto, Y., Kai, Y., Morinaga, H., Iga-Murahashi, M., Matsuyama, M., Sasaki, T., Maruyama, H., Shimotori, M., Makino, H., Sugiyama, H. et al. (2010) Fabry disease exhibiting recurrent stroke and persistent inflammation. Intern.Med., 49, 2247-2252.
34. Ong, C.T., Cheng, H.T., Chang, L.W., Ohtsuka, T., Kageyama, R., Stormo, G.D. and Kopan, R. (2006) Target selectivity of vertebrate notch proteins. Collaboration between discrete domains and CSL-binding site architecture determines activation probability. J. Biol. Chem., 281, 5106-5119.
35. van Breemen, M.J., Rombach, S.M., Dekker, N., Poorthuis, B.J., Linthorst, G.E., Zwinderman, A.H., Breunig, F., Wanner, C., Aerts, J.M. and Hollak, C.E. (2011) Reduction of elevated plasma globotriaosylsphingosine in patients with classic Fabry disease following enzyme replacement therapy. Biochim. Biophys. Acta, 1812, 70-76.
36. Golde, T.E., Koo, E.H., Felsenstein, K.M., Osborne, B.A. and Miele, L. (2013) gamma-Secretase inhibitors and modulators. Biochim. Biophys. Acta, 1828, 2898-2907.
37. Moreno, J.A., Moreno, S., Rubio-Navarro, A., Gomez-Guerrero, C., Ortiz, A. and Egido, J. (2014) Role of chemokines in proteinuric kidney disorders. Exp. Rev. Mol. Med., 16, e3.
38. Moreno, J.A., Moreno, S., Rubio-Navarro, A., Sastre, C., Blanco-Colio, L.M., Gomez-Guerrero, C., Ortiz, A. and Egido, J. (2012) Targeting chemokines in proteinuria-induced renal disease. Exp. Opin. Ther. Targets, 16, 833-845.
39. Sanz, A.B., Sanchez-Nino, M.D., Ramos, A.M., Moreno, J.A., Santamaria, B., Ruiz-Ortega, M., Egido, J. and Ortiz, A. (2010) NF-kappaB in renal inflammation. J. Am. Soc. Nephrol., 21, 1254-1262.
40. Sanz, A.B., Justo, P., Sanchez-Nino, M.D., Blanco-Colio, L.M., Winkles, J.A., Kreztler, M., Jakubowski, A., Blanco, J., Egido, J. and Ruiz-Ortega, M. et al. (2008) The cytokine TWEAK modulates renal tubulointerstitial inflammation. J. Am. Soc. Nephrol., 19, 695-703.
41. Wanner, C., Oliveira, J.P., Ortiz, A., Mauer, M., Germain, D.P., Linthorst, G.E., Serra, A.L., Marodi, L., Mignani, R., Cianciaruso, B. et al. (2010) Prognostic indicators of renal disease progression in adults with Fabry disease: natural history data from the Fabry Registry. Clin. J. Am. Soc. Nephrol., 5, 2220-2228.
42. Thurberg, B.L., Fallon, J.T., Mitchell, R., Aretz, T., Gordon, R.E. and O'Callaghan, M.W. (2009) Cardiac microvascular pathology in Fabry disease: evaluation of endomyocardial biopsies before and after enzyme replacement therapy. Circulation, 119, 2561-2567.
43. Boutin, M., Gagnon, R., Lavoie, P. and Auray-Blais, C. (2012) LC-MS/MS analysis of plasma lyso-Gb3 in Fabry disease. Clin. Chim. Acta, 414, 273-280.
44. Oqvist, B., Brenner, B.M., Oliveira, J.P., Ortiz, A., Schaefer, R., Svarstad, E., Wanner, C., Zhang, K. and Warnock, D.G. (2009) Nephropathy in Fabry disease: the importance of early diagnosis and testing in high-risk populations. Nephrol. Dial. Transpl., 24, 1736-1743.
45. Mauer, M., Glynn, E., Svarstad, E., Tondel, C., Gubler, M.C., West, M., Sokolovskiy, A., Whitley, C. and Najafian, B. (2014) Mosaicism of podocyte involvement is related to podocyte injury in females with Fabry disease. PLoS ONE, 9, e112188.
46. Iglesias-de la Cruz, M.C., Ziyadeh, F.N., Isono, M., Kouahou, M., Han, D.C., Kalluri, R., Mundel, P. and Chen, S. (2002) Effects of high glucose and TGF-beta1 on the expression of collagen IV and vascular endothelial growth factor in mouse podocytes. Kidney Int., 62, 901-913.
47. Nyhan, K.C., Faherty, N., Murray, G., Cooey, L.B., Godson, C., Crean, J.K. and Brazil, D.P. (2010) Jagged/Notch signalling is required for a subset of TGFbeta1 responses in human kidney epithelial cells. Biochim. Biophys. Acta, 1803, 1386-1395.
48. Lavoz, C., Droguett, A., Burgos, M.E., Carpio, D.J., Ortiz, A., Egido, J., Mezzano, S. and Ruiz-Ortega, M. (2014) Translational study of the Notch pathway in hypertensive nephropathy. Nefrologia, 34, 369-376.
49. Fogo, A.B., Bostad, L., Svarstad, E., Cook,W.J., Moll, S., Barbey, F., Geldenhuys, L., West, M., Ferluga, D., Vujkovac, B. et al. (2010) Scoring system for renal pathology in Fabry disease: report of the International Study Group of Fabry Nephropathy (ISGFN). Nephrol. Dial. Transpl., 25, 2168-2177.
50. Rastaldi, M.P., Armelloni, S., Berra, S., Calvaresi, N., Corbelli, A., Giardino, L.A., Li, M., Wang, G.Q., Fornasieri, A., Villa, A. et al. (2006) Glomerular podocytes contain neuron-like functional synaptic vesicles. FASEB J., 20, 976-978.
51. Zhang, Z., Yan, R., Zhang, Q., Li, J., Kang, X., Wang, H., Huan, L., Zhang, L., Li, F., Yang, S. et al. (2014) Hes1, a Notch signaling downstream target, regulates adult hippocampal neurogenesis following traumatic brain injury. Brain Res., 1583, 65-78.
52. Perez-Gomez, M.V., Sanchez-Niño, M.D., Sanz, A.B., Martín-Cleary, C., Ruiz-Ortega, M., Egido, J., Navarro-González, J.F., Ortiz, A. and Fernandez-Fernandez, B. (2015) Horizon 2020 in diabetic kidney disease: the clinical trial pipeline for addon therapies on top of renin angiotensin system blockade. J. Clin. Med., 4, 1325-1347.
53. Ferreira, S., Ortiz, A., Germain, D.P., Viana-Baptista, M., Caldeira-Gomes, A., Camprecios, M., Fenollar-Cortes, M., Gallegos-Villalobos, A., Garcia, D., Garcia-Robles, J.A. et al. (2015) The alpha-galactosidase A p.Arg118Cys variant does not cause a Fabry disease phenotype: data from individual patients and family studies. Mol. Genet. Metab., 114, 248-258.
54. Saleem, M.A., O'Hare, M.J., Reiser, J., Coward, R.J., Inward, C. D., Farren, T., Xing, C.Y., Ni, L., Mathieson, P.W. and Mundel, P. (2002) A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J. Am. Soc. Nephrol., 13, 630-638.
55. Sanchez-Nino, M.D., Poveda, J., Sanz, A.B., Carrasco, S., Ruiz-Ortega, M., Selgas, R., Egido, J. and Ortiz, A. (2014) 3,4-DGE is cytotoxic and decreases HSP27/HSPB1 in podocytes. Arch. Toxicol., 88, 597-608.
56. Sanchez-Nino, M.D., Poveda, J., Sanz, A.B., Mezzano, S., Carrasco, S., Fernandez-Fernandez, B., Burkly, L.C., Nair, V., Kretzler, M., Hodgin, J.B. et al. (2013) Fn14 in podocytes and proteinuric kidney disease. Biochim. Biophys. Acta, 1832, 2232-2243.
57. Sanchez-Nino, M.D., Sanz, A.B., Lorz, C., Gnirke, A., Rastaldi, M.P., Nair, V., Egido, J., Ruiz-Ortega, M., Kretzler, M. and Ortiz, A. (2010) BASP1 promotes apoptosis in diabetic nephropathy. J. Am. Soc. Nephrol., 21, 610-621.