GSK3, snail, and adhesion molecule regulation by cyclosporine a in renal tubular cells

Toxicological Sciences

Volumn 127, Issue 2, 2012, Pages 425-437

  Berzal, Sergio ^a   Alique, Matilde ^a   Ruiz Ortega, Marta ^a,b   Egido, Jesús ^b,c   Ortiz, Alberto ^b,c   Ramos, Adrián M ^a  

^a HOSPITAL UNIVERSITARIO FUNDACIÓN JIMÉNEZ DÍAZ   (Spain)

^b Section of Nephrology   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Adhesion proteins; Calcineurin inhibitors; Cyclosporin A; Epithelial mesenchymal transition; GSK3; Snail

Indexed keywords

BETA CATENIN; BINDING PROTEIN; CASPASE; CYCLOSPORIN A; GLYCOGEN SYNTHASE KINASE 3; LITHIUM; PROTEIN ZO1; SMALL INTERFERING RNA; TACROLIMUS; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; KIDNEY TUBULE CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

GASTROPODA; MURINAE;

EID: 84861471421     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs108     Document Type: Article

References (49)

1. Angres, B., Barth, A., and Nelson, W. J. (1996). Mechanism for transition from initial to stable cell-cell adhesion: Kinetic analysis of E-cadherinmediated adhesion using a quantitative adhesion assay. J. Cell Biol. 134, 549-557.
2. Bachelder, R. E., Yoon, S. O., Franci, C., Garcĺa de Herreros, A. G., and Mercurio, A. M. (2005). Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: Implications for the epithelial-mesenchymal transition. J. Cell Biol. 168, 29-33.
3. Barrallo-Gimeno, A., and Nieto, M. A. (2005). The Snail genes as inducers of cell movement and survival: Implications in development and cancer. Development 132, 3151-3161.
4. Boutet, A., De Frutos, C. A., Maxwell, P. H., Mayol, M. J., Romero, J., and Nieto, M. A. (2006). Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J. 25, 5603-5613.
5. Bubb, M. R., Senderowicz, A. M., Sausville, E. A., Duncan, K. L., and Korn, E. D. (1994). Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J. Biol. Chem. 269, 14869-14871.
6. Cano, A., Pérez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F., and Nieto, M. A. (2000). The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83.
7. Capaldo, C. T., and Macara, I. G. (2007). Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 18, 189-200.
8. Christ, M., McCartney-Francis, N. L., Kulkarni, A. B., Ward, J. M., Mizel, D. E., Mackall, C. L., Gress, R. E., Hines, K. L., Tian, H., and Karlsson, S. (1994). Immune dysregulation in TGF-beta 1-deficient mice. J. Immunol. 153, 1936-1946.
9. Clemens, M. J., Bushell, M., Jeffrey, I. W., Pain, V. M., and Morley, S. J. (2000). Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ. 7, 603-615.
10. Cohen, P., and Goedert, M. (2004). GSK3 inhibitors: Development and therapeutic potential. Nat. Rev. Drug Discov. 3, 479-487.
11. Docherty, N. G., ÓSullivan, O. E., Healy, D. A., Murphy, M., ÓNeill, A. J., Fitzpatrick, J. M., and Watson, R. W. (2006). TGF-beta1-induced EMT can occur independently of its proapoptotic effects and is aided by EGF receptor activation. Am. J. Physiol. Renal Physiol. 290, F1202-F1212.
12. Feldman, G., Kiely, B., Martin, N., Ryan, G., Mc Morrow, T., and Ryan, M. P. (2007). Role for TGF-beta in cyclosporine-induced modulation of renal epithelial barrier function. J. Am. Soc. Nephrol. 18, 1662-1671.
13. Gomez, I., Peña, C., Herrera, M., Muñoz, C., Larriba, M. J., Garcia, V., Domĺnguez, G., Silva, J., Rodrĺguez, R., Garcĺa de Herreros, A., et al. (2011). TWIST1 is expressed in colorectal carcinomas and predicts patient survival. PLoS One 6, e18023.
14. Grainger, D. J. (2004). Transforming growth factor beta and atherosclerosis: So far, so good for the protective cytokine hypothesis. Arterioscler. Thromb. Vasc. Biol. 24, 399-404.
15. Harney, A. S., Lee, J., Manus, L. M., Wang, P., Ballweg, D. M., LaBonne, C., and Meade, T. J. (2009). Targeted inhibition of Snail family zinc finger transcription factors by oligonucleotide-Co(III) Schiff base conjugate. Proc. Natl. Acad. Sci. U.S.A. 106, 13667-13672.
16. Hazzan, M., Hertig, A., Buob, D., Copin, M. C., Noël, C., Rondeau, E., and Dubois-Xu, Y. C. (2011). Epithelial-to-mesenchymal transition predicts cyclosporine nephrotoxicity in renal transplant recipients. J. Am. Soc. Nephrol. 22, 1375-1381.
17. Hertig, A., Flier, S. N., and Kalluri, R. (2010). Contribution of epithelial plasticity to renal transplantation-associated fibrosis. Transplant. Proc. 42, S7-S12.
18. Ito, H., Kasagi, N., Shomori, K., Osaki, M., and Adachi, H. (1995). Apoptosis in the human allografted kidney. Analysis by terminal deoxynucleotidyl transferase-mediated DUTP-botin nick end labeling. Transplantation 60, 794-798.
19. Ivanov, A. I. (2008). Actin motors that drive formation and disassembly of epithelial apical junctions. Front. Biosci. 13, 6662-6668.
20. Jeffrey, I. W., Bushell, M., Tilleray, V. J., Morley, S., and Clemens, M. J. (2002). Inhibition of protein synthesis in apoptosis: Differential requirements by the tumor necrosis factor alpha family and a DNA-damaging agent for caspases and the double-stranded RNA-dependent protein kinase. Cancer Res. 62, 2272-2280.
21. Jope, R. S., and Johnson, G. V. W. (2004). The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29, 95-102.
22. Justo, P., Lorz, C., Sanz, A., Egido, J., and Ortiz, A. (2003). Intracellular mechanisms of cyclosporin A-induced tubular cell apoptosis. J. Am. Soc. Nephrol. 14, 3072-3080.
23. Keller, S. H., and Nigam, S. K. (2003). Biochemical processing of E-cadherin under cellular stress. Biochem. Biophys. Res. Commun. 307, 215-223.
24. Lee, C. H., Kim, S., Kang, C. M., Kim, W. Y., Kim, J., and Kim, G. H. (2011). Altered expression of tight junction proteins in cyclosporine nephrotoxicity. Am. J. Nephrol. 33, 7-16.
25. Ling, H., Li, X., Jha, S., Wang, W., Karetskaya, L., Pratt, B., and Ledbetter, S. (2003). Therapeutic role of TGF-beta-neutralizing antibody in mousecyclosporin A nephropathy: Morphologic improvement associated with functional preservation. J. Am. Soc. Nephrol. 14, 377-388.
26. Liu, Y. (2010). New insights into epithelial-mesenchymal transition in kidney fibrosis. J. Am. Soc. Nephrol. 21, 212-222.
27. Martínez-Estrada, O. M., Cullerés, A., Soriano, F. X., Peinado, H., Bolós, V., Martínez, F. O., Reina, M., Cano, A., Fabre, M., Vilaró, S., et al. (2006). The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem. J. 394, 449-457.
28. McMorrow, T., Gaffney, M. M., Slattery, C., Campbell, E., and Ryan, M. P. (2005). Cyclosporine A induced epithelial-mesenchymal transition in human renal proximal tubular epithelial cells. Nephrol. Dial. Transplant. 20, 2215-2225.
29. Meijer, L., Flajolet, M., and Greengard, P. (2004). Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci. 25, 471-480.
30. Meran, S., and Steadman, R. (2011). Fibroblasts and myofibroblasts in renal fibrosis. Int. J. Exp. Pathol. 92, 158-167.
31. Moreno-Bueno, G., Cubillo, E., Sarrió, D., Peinado, H., Rodríguez-Pinilla, S. M., Villa, S., Bolós, V., Jordá, M., Fabra, A., Portillo, F., et al. (2006). Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epithelialmesenchymal transition. Cancer Res. 66, 9543-9556.
32. Moreno-Bueno, G., Portillo, F., and Cano, A. (2008). Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 27, 6958-6969.
33. Naesens, M., Kuypers, D. R. J., and Sarwal, M. (2009). Calcineurin inhibitor nephrotoxicity. Clin. J. Am. Soc. Nephrol. 4, 481-508.
34. Ohkubo, T., and Ozawa, M. (2004). The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J. Cell Sci. 117, 1675-1685.
35. Ortiz, A., Lorz, C., Catalán, M. P., Ortiz, A., Coca, S., and Egido, J. (1998). Cyclosporine A induces apoptosis in murine tubular epithelial cells: Role of caspases. Kidney Int. Suppl. 68, S25-S29.
36. Pallet, N., and Legendre, C. (2010). Deciphering calcineurin inhibitor nephrotoxicity: A pharmacological approach. Pharmacogenomics 11, 1491-1501.
37. Peinado, H., Olmeda, D., and Cano, A. (2007). Snail, Zeb and bHLH factors in tumour progression: An alliance against the epithelial phenotype? Nat. Rev. Cancer 7, 415-428.
38. Peinado, H., Portillo, F., and Cano, A. (2004). Transcriptional regulation of cadherins during development and carcinogenesis. Int. J. Dev. Biol. 48, 365-375.
39. Prozialeck, W. C., and Edwards, J. R. (2007). Cell adhesion molecules in chemically-induced renal injury. Pharmacol. Ther. 114, 74-93.
40. Sarró, E., Jacobs-Cachá, C., Itarte, E., and Meseguer, A. (2012). A pharmacologically-based array to identify targets of cyclosporine Ainduced toxicity in cultured renal proximal tubule cells. Toxicol. Appl. Pharmacol. 258, 275-287.
41. Seoane, J. (2006). Escaping from the TGFbeta anti-proliferative control. Carcinogenesis 27, 2148-2156.
42. Severson, E. A., Kwon, M., Hilgarth, R. S., Parkos, C. A., and Nusrat, A. (2010). Glycogen synthase kinase 3 (GSK-3) influences epithelial barrier function by regulating Occludin, Claudin-1 and E-cadherin expression. Biochem. Biophys. Res. Commun. 397, 592-597.
43. Slattery, C., Campbell, E., McMorrow, T., and Ryan, M. P. (2005). Cyclosporine A-induced renal fibrosis: A role for epithelial-mesenchymal transition. Am. J. Pathol. 167, 395-407.
44. Steinhusen, U., Weiske, J., Badock, V., Tauber, R., Bommert, K., and Huber, O. (2001). Cleavage and shedding of E-cadherin after induction of apoptosis. J. Biol. Chem. 276, 4972-4980.
45. Vega, S., Morales, A. V., Ocaña, O. H., Valdés, F., Fabregat, I., and Nieto, M. A. (2004). Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18, 1131-1143.
46. Viñas, J. L., Hotter, G., Pi, F., Palacios, L., and Sola, A. (2007). Role of peroxynitrite on cytoskeleton alterations and apoptosis in renal ischemiareperfusion. Am. J. Physiol. Renal Physiol. 292, F1673-F1680.
47. Wilson, P. D. (2011). Apico-basal polarity in polycystic kidney disease epithelia. Biochim. Biophys. Acta 1812, 1239-1248.
48. Zheng, G., Lyons, J. G., Tan, T. K., Wang, Y., Hsu, T. T., Min, D., Succar, L., Rangan, G. K., Hu, M., Henderson, B. R., et al. (2009). Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelialmesenchymal transition downstream of transforming growth factor-beta1 in renal tubular epithelial cells. Am. J. Pathol. 175, 580-591.
49. Zhou, B. P., Deng, J., Xia, W., Xu, J., Li, Y. M., and Gunduz, M. (2004). Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat. Cell Biol. 6, 931-940.