Concentrations of cyclosporin A and FK506 that inhibit IL-2 induction in human T cells do not affect TGF-β1 biosynthesis, whereas higher doses of cyclosporin A trigger apoptosis and release of preformed TGF-β1

Journal of Leukocyte Biology

Volumn 77, Issue 5, 2005, Pages 748-758

  Minguillón, Jordi ^a   Morancho, Beatriz ^a   Kim, Seong Jin ^b   López Botet, Miguel ^a   Aramburu, José ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Calcineurin; Immunosuppressants; Lymphocytes

Indexed keywords

CALCINEURIN INHIBITOR; CYCLOSPORIN A; INTERLEUKIN 2; PHORBOL 13 ACETATE 12 MYRISTATE; PHYTOHEMAGGLUTININ; T LYMPHOCYTE RECEPTOR; TACROLIMUS; TRANSFORMING GROWTH FACTOR BETA1;

APOPTOSIS; ARTICLE; CELL TYPE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MEGADOSE; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VIVO STUDY; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

APOPTOSIS; CALCINEURIN; CELLS, CULTURED; CYCLOSPORINE; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; T-LYMPHOCYTES; TACROLIMUS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

RODENTIA;

EID: 18244399071     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0904503     Document Type: Article

References (46)

1. Hogan, P. C., Chen, L., Nardone, J., Rao, A. (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17, 2205-2232.
2. Liu, J., Farmer Jr., J. D., Lane, W. S., Friedman, J., Weissman, I., Schreiber, S. L. (1991) Calcineurin is a common target of cyclophilin- cyclosporin A and FKBP-FK506 complexes. Cell 66, 807-815.
3. Aramburu, J., Rao, A., Klee, C. B. (2000) Calcineurin: from structure to function. Curr. Top. Cell. Regul. 36, 237-295.
4. Kiani, A., Rao, A., Aramburu, J. (2000) Manipulating immune responses with immunosuppressive agents that target NFAT. Immunity 12, 359-372.
5. Islam, M., Burke Jr., J. F.. McGowan, T. A., Zhu, Y., Dunn, S. R., McCue, P., Kanalas, J., Sharma, K. (2001) Effect of anti-transforming growth factor-β antibodies in cyclosporine-induced renal dysfunction. Kidney Int. 59, 498-506.
6. English, R. F., Pophal, S. A., Bacanu, S. A., Fricker, J., Boyle, G. J., Ellis, D., Harker, K., Sutton, R., Miller, S. A., Law, Y. M., Pigula, F. A., Webber, S. A. (2002) Long-term comparison of tacrolimus- and cyclosporine-induced nephrotoxicity in pediatric heart-transplant recipients. Am. J. Transplant. 2, 769-773.
7. Wolf, G., Thaiss, F., Stahl, R. A. (1995) Cyclosporine stimulate expression of transforming growth faotor-β in renal cells. Possible mechanism of cyclosporines antiproliferative effects. Transplantation 60, 237-241.
8. Prashar, Y., Khanna, A., Sehajpal, P., Sharma, V. K., Suthanthiran, M. (1995) Stimulation of transforming growth factor-β 1 transcription by cyclosporine. FEBS Lett. 358, 109-112.
9. Li, B., Sehajpal, P. K., Khanna, A., Vlassara, H., Cerami, A., Stenzel, K. H., Suthauthiran, M. (1991) Differential regulation of transforming growth factor β and interleukin 2 genes in human T cells: demonstration by usage of novel competitor DNA constructs in the quantitative polymerase chain reaction. J. Exp. Med. 174, 1259-1262.
10. Kulkarni, A. B., Huh, C. G., Becker, D., Geiser, A., Lyght, M., Flanders, K. C., Roberts, A. B., Sporn, M. B., Ward, J. M., Karlsson, S. (1993) Transforming growth factor β 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA 90, 770-774.
11. Waltenberger, J., Wanders, A., Fellstrom, B., Miyazono, K., Heldin, C. H., Funa, K. (1993) Induction of transforming growth factor-β during cardiac allograft rejection. J. Immunol. 151, 1147-1157.
12. Aharoni, R., Kayhan, B., Eilan, R., Sela, M., Arnon, R. (2003) Glatiramer acetate-specific T cells in the brain express T helper 2/3 cytokines and brain-derived neurotrophic factor in situ. Proc. Natl. Acad. Sci. USA 100, 14157-14162.
13. Liu, H., Hu, B., Xu, D., Liew, F. Y. (2003) CD4+ CD25+ regulatory T cells cure murine colitis: the role of IL-10, TGF-β, and CTLA4. J. Immunol. 171, 5012-5017.
14. Chen, W., Jin, W., Wahl, S. M. (1998) Engagement of cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) induces transforming growth factor β (TGF-β) production by murine CD4(+) T cells. J. Exp. Med. 188, 1849-1857.
15. Levings, M. K., Sangregorio, K., Sartirana, C., Moschin, A. L., Battaglia, M., Orban, P. C., Roncarolo, M. G. (2002) Human CD25+CD44+ T suppressor cell clones produce transforming growth factor β, but not interlenkin 10, and are distinct from type 1 T regulatory cells. J. Exp. Med. 196, 1335-1346.
16. Groux, H., O'Garra, A., Bigler, M., Rouleau, M., Antonenko, S., de Vries, J. E., Roncarolo, M. G. (1997) A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389, 737-742.
17. Fukaura, H., Kent, S. C., Pietrusewicz, M. J., Khoury, S. J., Weiner, H. L., Hafler, D. A. (1996) Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-β1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients. J. Clin. Invest. 98, 70-77.
18. Letterio, J. J., Ruberts, A. B. (1998) Regulation of immune responses by TCF-β. Annu. Rev. Immunol. 16, 137-161.
19. Chen, W., Frank, M. E., Jin, W., Wahl, S. M. (2001) TGF-β released by apoptotic T cells contributes to an immunosuppressive milien. Immunity 14, 715-725.
20. Spits, H., Keizer, G., Borst, J., Terhorst, C., Hekman, A., de Vries, J. E. (1983) Characterization of monoclonal antibodies against cell surface molecules associated with cytotoxic activity of natural and activated killer cells and cloned CTL lines. Hybridoma 2, 423-437.
21. Kim, S. J., Click, A., Sporn, M. B., Roberts, A. B. (1989) Characterization of the promoter region of the human transforming growth factor-β 1 gene. J. Biol. Chem. 264, 402-408.
22. Nordeen, S. K. (1988) Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques 6, 454-458.
23. Macian, F., Garcia-Rodriguez, C., Rao, A. (2000) Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. EMBO J. 19, 4783-4795.
24. Dolganov, G., Bort, S., Lovett, M., Burr, J., Schubert, L., Short, D., McGurn, M., Gibson, C., Lewis, D. B. (1996) Coexpression of the interleukin-13 and interleukin-4 genes correlates with their physical linkage in the cytokine gene cluster on human chromosome 5q23-31. Blood 87, 3316-3326.
25. Luo, C., Shaw, K. T., Raghavan, A., Aramburu, J., Garcia-Cozar, F., Perrino, B. A., Hogan, P. G., Rao, A. (1996) Interaction of calcineurin with a domain of the transcription factor NFATI that controls nuclear import. Proc. Natl. Acad. Sci. USA 93, 8907-8912.
26. Aramburu, J., Yaffe, M. B., Lopez-Rodriguez, C., Cantley, L. C., Hogan, P. G., Rao, A. (1999) Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285, 2129-2133.
27. Lopez-Rodriguez, C., Aramburu, J., Jin, L., Rakeman, A. S., Michino, M., Rao, A. (2001) Bridging the NFAT and NF-κB families: NFAT5 dimerization regulates cytokine gene transcription in response to osmotic stress. Immunity 15, 47-58.
28. Zhu, D., Cardenas, M. E., Heitman, J. (1996) Calcineurin mutants render T lymphocytes resistant to cyclosporin A. Mol. Pharmacol. 50, 506-511.
29. June, C. H., Ledbetter, J. A., Gillespie, M. M., Lindsten, T., Thompson, C. B. (1987) T-cell proliferation involving the CD28 pathway is associated with cyclosporine-resistant interleukin 2 gene expression. Mol. Cell. Biol. 7, 4472-4481.
30. Zawadzka, M., Kaninska, B. (2005) A novel mechanism of FK506-mediated neuroprotection: Downregulation of cytokine expression in glial cells. Glia 49, 36-51.
31. Khanna, A. K. (2003) The immunosuppressive agent tacrolimus induces p21WAF/CIP1WAF1/CIP1 via TGF-β secretion. Biochem. Biophys. Res. Commun. 303, 266-272.
32. Gooch, J. L., Barnes, J. L., Garcia, S., Abboud, H. E. (2003) Calcineurin is activated in diabetes and is required for glomerular hypertrophy and ECM accumulation. Am. J. Physiol. Renal Physiol. 284, F144-F154.
33. Kuprash, D. V., Boitchenko, V. E., Yarovinsky, F. O., Riee, N. R., Nordheim, A., Ruhlmann, A., Nedospasov, S. A. (2002) Cyclosporin A blocks the expression of lymphotoxin α, but not lymphotoxin β, in human peripheral blood mononuclear cells. Blood 100, 1721-1727.
34. Ahuja, S. S., Shrivastav, S., Danielpour, D., Balow, J. E., Boumpas, D. T. (1995) Regulation of transforming growth factor-β 1 and its receptor by cyclosporine in human T lymphocytes. Transplantation 60, 718-723.
35. Goppelt-Struebe, M., Esslinger, B., Kunzendorf, U. (2003) Failure ol cyclosporin A to induce transforming growth factor β(TGF-β) synthesis in activated peripheral blood lymphocytes. Clin. Transplant. 17, 20-25.
36. Wynn, C., Pan, F., Erickson, L., Ebbs, A., Kobayashi, M., Jiang, H. (2002) High level of TCF-β in organ transplantation might be due to rejection rather than calcineurin inhibitor medication. Transplant. Proc. 34, 1387-1389.
37. Hamar, P., Szabo, A., Muller, V., Heemann, U. (2002) The involvement of activated T cells and growth-factor production in the early and late phase of chronic kidney allograft nephropathy in rats. Transpl. Int. 15, 446-454.
38. Takahashi, K., Reynolds, M., Ogawa, N., Longo, D. L., Burdick, J. (2004) Augmentation of T-cell apoptosis by immunosuppressive agents. Clin. Transplant. 18 (Suppl. 12), 72-75.
39. Shihab, F. S., Bennett, W. M., Tanner, A. M., Andoh, T. F. (1997) Angiotensin II blockade decreases TGF-β1 and matrix proteins in cyclosporine nephropathy. Kidney Int. 52, 660-673.
40. Le Guellec, C., Buchler, M., Ciraudeuu, B., Le Meur, Y., Cakoue, J. E., Lebranchu, Y., Marquet, P., Paintaud, G. (2002) Simultaneous estimation of cyclosporin and mycophenolic acid areas under the curve in stable renal transplant patients using a limited sampling strategy. Eur. J. Clin. Pharmacol. 57, 805-811.
41. Hughes, J. R., Hughes, V. F., Trull, A. K., Metcalfe, S. M. (1999) Blood levels of TGF β1 in liver transplant recipients receiving either tacrolimus or micro-emulsified cyclosporine. Transplantation 68, 583-586.
42. Mohamed, M. A., Robertson, H., Booth, T. A., Balupuri, S., Kirhy, J. A., Talbot, D. (2000) TGF-β expression in renal transplant biopsies: a comparative study between cyclosporin-A and tacrolimus. Transplantation 69, 1002-1005.
43. Alvarez-Arroyo, M. V., Yague, S., Wenger, R. M., Pereira, D. S., Jimenez, S., Gonzalez-Pacheco, F. R., Castilla, M. A., Deudero, J. J., Caramelo, C. (2002) Cyclophilin-mediated pathways in the effect of cyclosporin A on endothelial cells: role of vascular endothelial growth factor. Circ. Res. 91, 202-209.
44. Hong, F., Lee, J., Song, J. W., Lee, S. J., Ahn, H., Cho, J. J., Ha, J., Kim, S. S. (2002) Cyclosporin A blocks muscle differentiation by inducing oxidative stress and inhibiting the peptidyl-prolyl-cis-trans isomerase activity of cyclophilin A: cyclophilin A protects myoblasts from cyclosporin A-induced cytotoxicity. FASEB J. 16, 1633-1635.
45. Healy, E., Dempsey, M., Lally, C., Ryan, M. P. (1998) Apoptosis and necrosis: mechanisms of cell death induced by cyclosporine A in a renal proximal tubular cell line. Kidney Int. 54, 1955-1966.
46. Hong, F., Lee, J., Piao, Y. J., Jae, Y. K., Kim, Y. J., Oh, C., Seo, J. S., Yun, Y. S., Yang, C. W., Ha, J., Kim, S. S. (2004) Transgenic mice overexpressing cyclophilin A are resistant to cyclosporin A-induced nephrotoxicity via peptidyl-prolyl cis-trans isomerase activity. Biochem. Biophys. Res. Commun. 316, 1073-1080.