Mapping cyclosporine-induced changes in protein secretion by renal cells using stable isotope labeling with amino acids in cell culture (SILAC)

Journal of Proteomics

Volumn 75, Issue 12, 2012, Pages 3674-3687

  Lamoureux, F ^a,b,c   Gastinel, L N ^a   Mestre, E ^a   Marquet, P ^a,b   Essig, M ^a,b  

^a INSERM   (France)

^b LIMOGES UNIVERSITY HOSPITAL   (France)

^c ROUEN UNIVERSITY HOSPITAL   (France)

Author keywords

Cyclosporine; Kidney; Proteomics; Secretome; SILAC; Toxicity

Indexed keywords

ACETYLCYSTEINE; ADAMTS1 PROTEIN; AMINO ACID; COLLAGEN TYPE 1; CYCLOPHILIN; CYCLOSPORIN; CYSTATIN C; DISINTEGRIN; ENTACTIN; FIBRONECTIN; LACTADHERIN; MACROPHAGE MIGRATION INHIBITION FACTOR; METALLOPROTEINASE; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN;

ARTICLE; CELL ADHESION; CELL STRAIN HEK293; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NEPHROTOXICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; UPREGULATION;

AMINO ACIDS; CELL ADHESION MOLECULES; CELLS, CULTURED; CYCLOPHILIN A; CYCLOPHILINS; CYCLOSPORINE; DOWN-REGULATION; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; ISOTOPE LABELING; KIDNEY; PROTEOME; UP-REGULATION;

EID: 84862206139     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.04.024     Document Type: Article

References (44)

1. Fireman M., DiMartini A.F., Armstrong S.C., Cozza K.L. Immunosuppressants. Psychosomatics 2004, 45:354-360.
2. Halloran P.F. Immunosuppressive drugs for kidney transplantation. N Engl J Med 2004, 351:2715-2729.
3. Myers B.D., Ross J., Newton L., Luetscher J., Perlroth M. Cyclosporine-associated chronic nephropathy. N Engl J Med 1984, 311:699-705.
4. Nankivell B.J., Borrows R.J., Fung C.L., O'Connell P.J., Allen R.D., Chapman J.R. The natural history of chronic allograft nephropathy. N Engl J Med 2003, 349:2326-2333.
5. Naesens M., Kuypers D.R., Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009, 4:481-508.
6. Justo P., Lorz C., Sanz A., Egido J., Ortiz A. Intracellular mechanisms of cyclosporin A-induced tubular cell apoptosis. J Am Soc Nephrol 2003, 14:3072-3080.
7. Hortelano S., Castilla M., Torres A.M., Tejedor A., Bosca L. Potentiation by nitric oxide of cyclosporin A and FK506-induced apoptosis in renal proximal tubule cells. J Am Soc Nephrol 2000, 11:2315-2323.
8. Kurtz A., Della B.R., Kuhn K. Cyclosporine A enhances renin secretion and production in isolated juxtaglomerular cells. Kidney Int 1988, 33:947-953.
9. Bouvier N., Flinois J.P., Gilleron J., Sauvage F.L., Legendre C., Beaune P., et al. Cyclosporine triggers endoplasmic reticulum stress in endothelial cells: a role for endothelial phenotypic changes and death. Am J Physiol Renal Physiol 2009, 296:F160-F169.
10. Pallet N., Bouvier N., Legendre C., Gilleron J., Codogno P., Beaune P., et al. Autophagy protects renal tubular cells against cyclosporine toxicity. Autophagy 2008, 4:783-791.
11. Pallet N., Rabant M., Xu-Dubois Y.C., Lecorre D., Mucchielli M.H., Imbeaud S., et al. Response of human renal tubular cells to cyclosporine and sirolimus: a toxicogenomic study. Toxicol Appl Pharmacol 2008, 229:184-196.
12. Wolf A., Trendelenburg C.F., ez-Fernandez C., Prieto P., Houy S., Trommer W.E., et al. Cyclosporine A-induced oxidative stress in rat hepatocytes. J Pharmacol Exp Ther 1997, 280:1328-1334.
13. Zhong Z., Arteel G.E., Connor H.D., Yin M., Frankenberg M.V., Stachlewitz R.F., et al. Cyclosporin A increases hypoxia and free radical production in rat kidneys: prevention by dietary glycine. Am J Physiol 1998, 275:F595-F604.
14. Tariq M., Morais C., Sobki S., Al S.M., Al K.A. N-acetylcysteine attenuates cyclosporin-induced nephrotoxicity in rats. Nephrol Dial Transplant 1999, 14:923-929.
15. Wang C., Salahudeen A.K. Cyclosporine nephrotoxicity: attenuation by an antioxidant-inhibitor of lipid peroxidation in vitro and in vivo. Transplantation 1994, 58:940-946.
16. Puigmule M., Lopez-Hellin J., Sune G., Tornavaca O., Camano S., Tejedor A., et al. Differential proteomic analysis of cyclosporine A-induced toxicity in renal proximal tubule cells. Nephrol Dial Transplant 2009, 24:2672-2686.
17. Molloy M.P., Brzezinski E.E., Hang J., McDowell M.T., VanBogelen R.A. Overcoming technical variation and biological variation in quantitative proteomics. Proteomics 2003, 3:1912-1919.
18. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 2002, 1:376-386.
19. Dong X., Xiong L., Jiang X., Wang Y. Quantitative proteomic analysis reveals the perturbation of multiple cellular pathways in jurkat-T cells induced by doxorubicin. J Proteome Res 2010, 9:5943-5951.
20. Lamoureux F., Mestre E., Essig M., Sauvage F.L., Marquet P., Gastinel L.N. Quantitative proteomic analysis of cyclosporine-induced toxicity in a human kidney cell line and comparison with tacrolimus. J Proteomics 2011, 2:677-694.
21. Xiong L., Wang Y. Quantitative proteomic analysis reveals the perturbation of multiple cellular pathways in HL-60 cells induced by arsenite treatment. J Proteome Res 2010, 9:1129-1137.
22. Ong S.E., Mann M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc 2006, 1:2650-2660.
23. Bendall S.C., Hughes C., Stewart M.H., Doble B., Bhatia M., Lajoie G.A. Prevention of amino acid conversion in SILAC experiments with embryonic stem cells. Mol Cell Proteomics 2008, 7:1587-1597.
24. Huang dW, Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
25. Nashan B., Cole E., Levy G., Thervet E. Clinical validation studies of Neoral C(2) monitoring: a review. Transplantation 2002, 73:S3-S11.
26. Kruger M., Kratchmarova I., Blagoev B., Tseng Y.H., Kahn C.R., Mann M. Dissection of the insulin signaling pathway via quantitative phosphoproteomics. Proc Natl Acad Sci U S A 2008, 105:2451-2456.
27. Jennings P., Aydin S., Bennett J., McBride R., Weiland C., Tuite N., et al. Inter-laboratory comparison of human renal proximal tubule (HK-2) transcriptome alterations due to Cyclosporine A exposure and medium exhaustion. Toxicol In Vitro 2009, 23:486-499.
28. O'Connell S., Slattery C., Ryan M.P., McMorrow T. Identification of novel indicators of cyclosporine A nephrotoxicity in a CD-1 mouse model. Toxicol Appl Pharmacol 2011, 252:201-210.
29. Price E.R., Jin M., Lim D., Pati S., Walsh C.T., McKeon F.D. Cyclophilin B trafficking through the secretory pathway is altered by binding of cyclosporin A. Proc Natl Acad Sci U S A 1994, 91:3931-3935.
30. Yurchenko V., Constant S., Eisenmesser E., Bukrinsky M. Cyclophilin-CD147 interactions: a new target for anti-inflammatory therapeutics. Clin Exp Immunol 2010, 160:305-317.
31. Price E.R., Zydowsky L.D., Jin M.J., Baker C.H., McKeon F.D., Walsh C.T. Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence. Proc Natl Acad Sci U S A 1991, 88:1903-1907.
32. Swanson S.K., Born T., Zydowsky L.D., Cho H., Chang H.Y., Walsh C.T., et al. Cyclosporin-mediated inhibition of bovine calcineurin by cyclophilins A and B. Proc Natl Acad Sci U S A 1992, 89:3741-3745.
33. Jin Z.G., Melaragno M.G., Liao D.F., Yan C., Haendeler J., Suh Y.A., et al. Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ Res 2000, 87:789-796.
34. Pallet N., Bouvier N., Bendjallabah A., Rabant M., Flinois J.P., Hertig A., et al. Cyclosporine-induced endoplasmic reticulum stress triggers tubular phenotypic changes and death. Am J Transplant 2008, 8:2283-2296.
35. Kato N., Kosugi T., Sato W., Ishimoto T., Kojima H., Sato Y., et al. Basigin/CD147 promotes renal fibrosis after unilateral ureteral obstruction. Am J Pathol 2011, 178:572-579.
36. De C.F., Allain F., Caliez A., Spik G., Vanhoutte P.M. High binding capacity of cyclophilin B to chondrocyte heparan sulfate proteoglycans and its release from the cell surface by matrix metalloproteinases: possible role as a proinflammatory mediator in arthritis. Arthritis Rheum 2003, 48:2197-2206.
37. Peng H., Vijayakumar S., Schiene-Fischer C., Li H., Purkerson J.M., Malesevic M., et al. Secreted cyclophilin A, a peptidylprolyl cis-trans isomerase, mediates matrix assembly of hensin, a protein implicated in epithelial differentiation. J Biol Chem 2009, 284:6465-6475.
38. Decramer S., Rbig Z.U., Wittke S., Mischak H., Bascands J.L., Schanstra J.P. Identification of urinary biomarkers by proteomics in newborns: use in obstructive nephropathy. Contrib Nephrol 2008, 160:127-141.
39. Fricker L.D., McKinzie A.A., Sun J., Curran E., Qian Y., Yan L., et al. Identification and characterization of proSAAS, a granin-like neuroendocrine peptide precursor that inhibits prohormone processing. J Neurosci 2000, 20:639-648.
40. Murray B.M., Paller M.S., Ferris T.F. Effect of cyclosporine administration on renal hemodynamics in conscious rats. Kidney Int 1985, 28:767-774.
41. Duru M., Nacar A., Yonden Z., Kuvandik G., Helvaci M.R., Koc A., et al. Protective effects of N-acetylcysteine on cyclosporine-A-induced nephrotoxicity. Ren Fail 2008, 30:453-459.
42. Sune G., Sarro E., Puigmule M., Lopez-Hellin J., Zufferey M., Pertel T., et al. Cyclophilin B interacts with sodium-potassium ATPase and is required for pump activity in proximal tubule cells of the kidney. PLoS One 2010, 5:e13930.
43. Stemmy E.J., Benton A.S., Lerner J., Alcala S., Constant S.L., Freishtat R.J. Extracellular cyclophilin levels associate with parameters of asthma in phenotypic clusters. J Asthma 2011, 48:986-993.
44. Stemmy E.J., Balsley M.A., Jurjus R.A., Damsker J.M., Bukrinsky M.I., Constant S.L. Blocking cyclophilins in the chronic phase of asthma reduces the persistence of leukocytes and disease reactivation. Am J Respir Cell Mol Biol 2011, 45:991-998.