Calcineurin inhibitors: 40 Years later, can't live without...

Journal of Immunology

Volumn 191, Issue 12, 2013, Pages 5785-5791

  Azzi, Jamil R ^a   Sayegh, Mohamed H ^a,b   Mallat, Samir G ^b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; CALCINEURIN INHIBITOR; CYCLOPHILIN; CYCLOSPORIN; IMMUNOPHILIN; PHOSPHATASE; PLACEBO; PREDNISOLONE; TACROLIMUS; TRANSCRIPTION FACTOR NFAT;

ASPERGILLOSIS; ATOPIC DERMATITIS; BRAIN DISEASE; CAUSE OF DEATH; CELL PROLIFERATION; CEREBRAL BLINDNESS; CREATININE BLOOD LEVEL; CROHN DISEASE; DIABETES MELLITUS; DRUG DOSE INCREASE; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG SAFETY; DRY EYE; DYSLIPIDEMIA; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRAPYRAMIDAL SYNDROME; EYE INJURY; FIBROGENESIS; GINGIVA HYPERPLASIA; GRAFT FAILURE; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; HEADACHE; HEMAGGLUTINATION INHIBITION TEST; HIRSUTISM; HUMAN; KERATOCONJUNCTIVITIS; KIDNEY DISEASE; KIDNEY INJURY; LEUKOENCEPHALOPATHY; LIVER FAILURE; LOW DRUG DOSE; MYASTHENIA GRAVIS; NEPHROTOXICITY; NONHUMAN; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; PSORIASIS; PYELONEPHRITIS; REVIEW; RHEUMATOID ARTHRITIS; SEIZURE; SJOEGREN SYNDROME; SKIN DEFECT; SURVIVAL RATE; T LYMPHOCYTE ACTIVATION; TREMOR; UNSPECIFIED SIDE EFFECT; UVEITIS; VASCULAR DISEASE; VASOCONSTRICTION;

EID: 84890370392     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1390055     Document Type: Review

References (81)

1. Kapturczak, M. H., H. U. Meier-Kriesche, and B. Kaplan. 2004. Pharmacology of calcineurin antagonists. Transplant. Proc. 36(2, Suppl.): 25S-32S.
2. Kolata, G. 1983. Drug transforms transplant medicine. Science 221: 40-42.
3. Zand, M. S. 2005. Immunosuppression and immune monitoring after renal transplantation. Semin. Dial. 18: 511-519.
4. Heusler, K., and A. Pletscher. 2001. The controversial early history of cyclosporin. Swiss Med. Wkly. 131: 299-302.
5. Borel, J. F. 2002. History of the discovery of cyclosporin and of its early pharmacological development. Wien. Klin. Wochenschr. 114: 433-437.
6. Borel, J. F., C. Feurer, H. U. Gubler, and H. Stähelin. 1976. Biological effects of cyclosporin A: a new antilymphocytic agent. Agents Actions 6: 468-475.
7. Bram, R. J., D. T. Hung, P. K. Martin, S. L. Schreiber, and G. R. Crabtree. 1993. Identification of the immunophilins capable of mediating inhibition of signal transduction by cyclosporin A and FK506: roles of calcineurin binding and cellular location. Mol. Cell. Biol. 13: 4760-4769.
8. Hurwitz, M. Y., J. A. Putkey, C. B. Klee, and A. R. Means. 1988. Domain II of calmodulin is involved in activation of calcineurin. FEBS Lett. 238: 82-86.
9. Klee, C. B., G. F. Draetta, and M. J. Hubbard. 1988. Calcineurin. Adv. Enzymol. Relat. Areas Mol. Biol. 61: 149-200.
10. Shenolikar, S. 1994. Protein serine/threonine phosphatases: new avenues for cell regulation. Annu. Rev. Cell Biol. 10: 55-86.
11. Zhang, B. W., G. Zimmer, J. Chen, D. Ladd, E. Li, F. W. Alt, G. Wiederrecht, J. Cryan, E. A. O'Neill, C. E. Seidman, et al. 1996. T cell responses in calcineurin A alpha-deficient mice. J. Exp. Med. 183: 413-420.
12. Rao, A., C. Luo, and P. G. Hogan. 1997. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15: 707-747.
13. Shibasaki, F., E. R. Price, D. Milan, and F. McKeon. 1996. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382: 370-373.
14. Miroux, C., O. Moralès, A. Carpentier, S. Dharancy, F. Conti, E. Boleslowski, P. Podevin, C. Auriault, V. Pancré, and N. Delhem. 2009. Inhibitory effects of cyclosporine on human regulatory T cells in vitro. Transplant. Proc. 41: 3371-3374.
15. Miroux, C., O. Morales, K. Ghazal, S. B. Othman, Y. de Launoit, V. Pancré, F. Conti, and N. Delhem. 2012. In vitro effects of cyclosporine A and tacrolimus on regulatory T-cell proliferation and function. Transplantation 94: 123-131.
16. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell 133: 775-787.
17. Stähelin, H. F. 1996. The history of cyclosporin A (Sandimmune) revisited: another point of view. Experientia 52: 5-13.
18. Calne, R. Y. 1977. Renal transplantation. Lancet 2: 1283-1284.
19. Calne, R. Y., D. J. White, K. Rolles, D. P. Smith, and B. M. Herbertson. 1978. Prolonged survival of pig orthotopic heart grafts treated with cyclosporin A. Lancet 1: 1183-1185.
20. Green, C. J., and A. C. Allison. 1978. Extensive prolongation of rabbit kidney allograft survival after short-term cyclosporin-A treatment. Lancet 1: 1182-1183.
21. Calne, R. Y., D. J. White, S. Thiru, D. B. Evans, P. McMaster, D. C. Dunn, G. N. Craddock, B. D. Pentlow, and K. Rolles. 1978. Cyclosporin A in patients receiving renal allografts from cadaver donors. Lancet 2: 1323-1327.
22. Powles, R. L., A. J. Barrett, H. Clink, H. E. Kay, J. Sloane, and T. J. McElwain. 1978. Cyclosporin A for the treatment of graft-versus-host disease in man. Lancet 2: 1327-1331.
23. Calne, R. Y., K. Rolles, D. J. White, S. Thiru, D. B. Evans, P. McMaster, D. C. Dunn, G. N. Craddock, R. G. Henderson, S. Aziz, and P. Lewis. 1979. Cyclosporin A initially as the only immunosuppressant in 34 recipients of cadaveric organs: 32 kidneys, 2 pancreases, and 2 livers. Lancet 2: 1033-1036.
24. Starzl, T. E., G. B. Klintmalm, K. A. Porter, S. Iwatsuki, and G. P. Schröter. 1981. Liver transplantation with use of cyclosporin a and prednisone. N. Engl. J. Med. 305: 266-269.
25. 1983. Cyclosporin in cadaveric renal transplantation: one-year follow-up of a multicentre trial. Lancet 2: 986-989.
26. 1983. A randomized clinical trial of cyclosporine in cadaveric renal transplantation. N. Engl. J. Med. 309: 809-815.
27. Opelz, G. 1986. Multicenter impact of ciclosporin on cadaver kidney graft survival. Prog. Allergy 38: 329-345.
28. Reece, I. J., O. H. Frazier, A. Painvin, O. J. Okereke, L. B. Chandler, T. W. Krudewig, and D. A. Cooley. 1984. Early results of cardiac transplantation at the Texas Heart Institute. Thorax 39: 676-680.
29. Schäfers, H. J., A. Haverich, T. O. Wagner, M. M. Höper, T. Wahlers, B. Heublein, H. Fabel, and H. G. Borst. 1990. [Unilateral lung transplantation: a new perspective in the treatment of pulmonary fibrosis]. Pneumologie 44: 943-949.
30. Toronto Lung Transplant Group. 1986. Unilateral lung transplantation for pulmonary fibrosis. N. Engl. J. Med. 314: 1140-1145.
31. Sayegh, M. H., and C. B. Carpenter. 2004. Transplantation 50 years later: progress, challenges, and promises. N. Engl. J. Med. 351: 2761-2766.
32. Førre, O., K. Waalen, H. E. Rugstad, K. J. Berg, D. Solbu, and E. Kåss. 1988. Cyclosporine and rheumatoid arthritis. Springer Semin. Immunopathol. 10: 263-277.
33. Mueller, W., and B. Herrmann. 1979. Cyclosporin A for psoriasis. N. Engl. J. Med. 301: 555-556.
34. Ellis, C. N., M. S. Fradin, J. M. Messana, M. D. Brown, M. T. Siegel, A. H. Hartley, L. L. Rocher, S. Wheeler, T. A. Hamilton, T. G. Parish, et al. 1991. Cyclosporine for plaque-type psoriasis. Results of a multidose, double-blind trial. N. Engl. J. Med. 324: 277-284.
35. Førre, O., F. Bjerkhoel, C. F. Salvesen, K. J. Berg, H. E. Rugstad, G. Saelid, O. J. Mellbye, and E. Kåss. 1987. An open, controlled, randomized comparison of cyclosporine and azathioprine in the treatment of rheumatoid arthritis: a preliminary report. Arthritis Rheum. 30: 88-92.
36. Frey, F. J. 1990. [Cyclosporin in autoimmune diseases]. Schweiz. Med. Wochenschr. 120: 772-786.
37. Tejani, A. 1987. Cyclosporine treatment in patients with primary glomerular diseases. Int. J. Pediatr. Nephrol. 8: 1-3.
38. Meyrier, A. 2003. Treatment of idiopathic nephrosis by immunophillin modulation. Nephrol. Dial. Transplant. 18(Suppl. 6): vi79-vi86.
39. Ponticelli, C., G. Rizzoni, A. Edefonti, P. Altieri, E. Rivolta, S. Rinaldi, L. Ghio, E. Lusvarghi, R. Gusmano, F. Locatelli, et al. 1993. A randomized trial of cyclosporine in steroid-resistant idiopathic nephrotic syndrome. Kidney Int. 43: 1377-1384.
40. Cattran, D. C., G. B. Appel, L. A. Hebert, L. G. Hunsicker, M. A. Pohl, W. E. Hoy, D. R. Maxwell, and C. L. Kunis; North America Nephrotic Syndrome Study Group. 2001. Cyclosporine in patients with steroid-resistant membranous nephropathy: a randomized trial. Kidney Int. 59: 1484-1490.
41. Praga, M., V. Barrio, G. F. Juárez, and J. Luño; Grupo Español de Estudio de la Nefropatía Membranosa. 2007. Tacrolimus monotherapy in membranous nephropathy: a randomized controlled trial. Kidney Int. 71: 924-930.
42. Klein, M., J. Radhakrishnan, and G. Appel. 1999. Cyclosporine treatment of glomerular diseases. Annu. Rev. Med. 50: 1-15.
43. Gupta, A. K., M. D. Brown, C. N. Ellis, L. L. Rocher, G. J. Fisher, O. Baadsgaard, K. D. Cooper, and J. J. Voorhees. 1989. Cyclosporine in dermatology. J. Am. Acad. Dermatol. 21: 1245-1256.
44. Utine, C. A., M. Stern, and E. K. Akpek. 2010. Clinical review: topical ophthalmic use of cyclosporin A. Ocul. Immunol. Inflamm. 18: 352-361.
45. Hanifin, J. M., M. R. Ling, R. Langley, D. Breneman, and E. Rafal. 2001. Tacrolimus ointment for the treatment of atopic dermatitis in adult patients: part I, efficacy. J. Am. Acad. Dermatol. 44(1, Suppl.): S28-S38.
46. van den Hoogen, M., and L. Hilbrands. 2008. Reduced exposure to calcineurin inhibitors in renal transplantation. N. Engl. J. Med. 358: 2519.
47. Ekberg, H., H. Tedesco-Silva, A. Demirbas, S. Vítko, B. Nashan, A. Gürkan, R. Margreiter, C. Hugo, J. M. Grinyó, U. Frei, et al ELITE-Symphony Study. 2007. Reduced exposure to calcineurin inhibitors in renal transplantation. N. Engl. J. Med. 357: 2562-2575.
48. Borel, J. F., C. Feurer, H. U. Gubler, and H. Stähelin. 1994. Biological effects of cyclosporin A: a new antilymphocytic agent. 1976. Agents Actions 43: 179-186.
49. Borello, B. 1999. [Histories of the history of women]. Clio 35: 343-352.
50. D'Alfonso, S., I. Borelli, A. Dall'Omo, E. Bolognesi, J. Partanen, A. Levo, F. Pociot, L. Fan, T. Juji, M. Hammond, et al. 1998. The natural history of an HLA haplotype and its recombinants. Immunogenetics 48: 8-15.
51. Nankivell, B. J., R. J. Borrows, C. L. Fung, P. J. O'Connell, R. D. Allen, and J. R. Chapman. 2003. The natural history of chronic allograft nephropathy. N. Engl. J. Med. 349: 2326-2333.
52. Schmid, F. X. 1995. Protein folding. Prolyl isomerases join the fold. Curr. Biol. 5: 993-994.
53. Soter, N. A., A. B. Fleischer, Jr, G. F. Webster, E. Monroe, and I. Lawrence. 2001. Tacrolimus ointment for the treatment of atopic dermatitis in adult patients: part II, safety. J. Am. Acad. Dermatol. 44(1, Suppl.): S39-S46.
54. Utine, C. A. 2011. Update and critical appraisal of the use of topical azithromycin ophthalmic 1% (AzaSite) solution in the treatment of ocular infections. Clin. Ophthalmol. 5: 801-809.
55. Serón, D., F. Moreso, X. Fulladosa, M. Hueso, M. Carrera, and J. M. Grinyó. 2002. Reliability of chronic allograft nephropathy diagnosis in sequential protocol biopsies. Kidney Int. 61: 727-733.
56. Joy, M. S., V. Nickeleit, S. L. Hogan, B. D. Thompson, and W. F. Finn. 2005. Calcineurin inhibitor-induced nephrotoxicity and renal expression of P-glycoprotein. Pharmacotherapy 25: 779-789.
57. Ishikura, K., M. Ikeda, Y. Hamasaki, H. Hataya, S. Shishido, H. Asanuma, G. Nishimura, R. Hiramoto, and M. Honda. 2006. Posterior reversible encephalopathy syndrome in children: its high prevalence and more extensive imaging findings. Am. J. Kidney Dis. 48: 231-238.
58. Bagnis, C., G. Deray, M. Dubois, Y. Adabra, C. Jacquiaud, M. C. Jaudon, and C. Jacobs. 1997. Comparative acute nephrotoxicity of FK-506 and ciclosporin in an isolated in situ autoperfused rat kidney model. Am. J. Nephrol. 17: 17-24.
59. Jain, S., G. R. Bicknell, and M. L. Nicholson. 2000. Tacrolimus has less fibrogenic potential than cyclosporin A in a model of renal ischaemia- reperfusion injury. Br. J. Surg. 87: 1563-1568.
60. Heisel, O., R. Heisel, R. Balshaw, and P. Keown. 2004. New onset diabetes mellitus in patients receiving calcineurin inhibitors: a systematic review and meta-analysis. Am. J. Transplant. 4: 583-595.
61. Williams, D., and L. Haragsim. 2006. Calcineurin nephrotoxicity. Adv. Chronic Kidney Dis. 13: 47-55.
62. Pirsch, J. D., J. Miller, M. H. Deierhoi, F. Vincenti, and R. S. Filo. 1997. A comparison of tacrolimus (FK506) and cyclosporine for immunosuppression after cadaveric renal transplantation. FK506 Kidney Transplant Study Group. Transplantation 63: 977-983.
63. Sonoda, T., S. Takahara, K. Takahashi, K. Uchida, S. Ohshima, H. Toma, K. Tanabe, and N. Yoshimura; Japanese Tacrolimus Study Group. 2003. Outcome of 3 years of immunosuppression with tacrolimus in more than 1,000 renal transplant recipients in japan. Transplantation 75: 199-204.
64. Ekberg, H., C. Bernasconi, H. Tedesco-Silva, S. Vitko, C. Hugo, A. Demirbas, R. R. Acevedo, J. Grinyô, U. Frei, Y. Vanrenterghem, P. Daloze, and P. Halloran. 2009. Calcineurin inhibitor minimization in the Symphony study: observational results 3 years after transplantation. Am. J. Transplant. 9: 1876-1885.
65. Woodward, R. S., A. Kutinova, M. A. Schnitzler, and D. C. Brennan. 2005. Renal graft survival and calcineurin inhibitor. Transplantation 80: 629-633.
66. Goldfarb-Rumyantzev, A. S., L. Smith, F. S. Shihab, B. C. Baird, A. N. Habib, S. J. Lin, and L. L. Barenbaum. 2006. Role of maintenance immunosuppressive regimen in kidney transplant outcome. Clin. J. Am. Soc. Nephrol. 1: 563-574.
67. Boyer, O., J. Le Bidois, M. Dechaux, M. C. Gubler, and P. Niaudet. 2005. Improvement of renal function in pediatric heart transplant recipients treated with lowdose calcineurin inhibitor and mycophenolate mofetil. Transplantation 79: 1405-1410.
68. Mulay, A. V., S. Cockfield, R. Stryker, D. Fergusson, and G. A. Knoll. 2006. Conversion from calcineurin inhibitors to sirolimus for chronic renal allograft dysfunction: a systematic review of the evidence. Transplantation 82: 1153-1162.
69. Wali, R. K., V. Mohanlal, E. Ramos, S. Blahut, C. Drachenberg, J. Papadimitriou, M. Dinits, A. Joshi, B. Philosophe, C. Foster, et al. 2007. Early withdrawal of calcineurin inhibitors and rescue immunosuppression with sirolimus-based therapy in renal transplant recipients with moderate to severe renal dysfunction. Am. J. Transplant. 7: 1572-1583.
70. Vincenti, F., B. Charpentier, Y. Vanrenterghem, L. Rostaing, B. Bresnahan, P. Darji, P. Massari, G. A. Mondragon-Ramirez, M. Agarwal, G. Di Russo, et al. 2010. A phase III study of belatacept-based immunosuppression regimens versus cyclosporine in renal transplant recipients (BENEFIT study). Am. J. Transplant. 10: 535-546.
71. Durrbach, A., J. M. Pestana, T. Pearson, F. Vincenti, V. D. Garcia, J. Campistol, C. Rial Mdel, S. Florman, A. Block, G. Di Russo, et al. 2010. A phase III study of belatacept versus cyclosporine in kidney transplants from extended criteria donors (BENEFIT-EXT study). Am. J. Transplant. 10: 547-557.
72. Dharnidharka, V. R. 2005. Costimulation blockade with belatacept in renal transplantation. N. Engl. J. Med. 353: 2085-2086.
73. Vincenti, F., C. Larsen, A. Durrbach, T. Wekerle, B. Nashan, G. Blancho, P. Lang, J. Grinyo, P. F. Halloran, K. Solez, et al; Belatacept Study Group. 2005. Costimulation blockade with belatacept in renal transplantation. N. Engl. J. Med. 353: 770-781.
74. Sharif, A., S. Shabir, S. Chand, P. Cockwell, S. Ball, and R. Borrows. 2011. Meta-analysis of calcineurin-inhibitor-sparing regimens in kidney transplantation. J. Am. Soc. Nephrol. 22: 2107-2118.
75. Schena, F. P., M. D. Pascoe, J. Alberu, M. del Carmen Rial, R. Oberbauer, D. C. Brennan, J. M. Campistol, L. Racusen, M. S. Polinsky, R. Goldberg-Alberts, et al; Sirolimus CONVERT Trial Study Group. 2009. Conversion from calcineurin inhibitors to sirolimus maintenance therapy in renal allograft recipients: 24-month efficacy and safety results from the CONVERT trial. Transplantation 87: 233-242.
76. El-Charabaty, E., A. S. Geara, C. Ting, S. El-Sayegh, and J. Azzi. 2012. Belatacept: a new era of immunosuppression? Expert Rev. Clin. Immunol. 8: 527-536.
77. Vincenti, F., G. Blancho, A. Durrbach, P. Friend, J. Grinyo, P. F. Halloran, J. Klempnauer, P. Lang, C. P. Larsen, F. Mühlbacher, et al. 2010. Five-year safety and efficacy of belatacept in renal transplantation. J. Am. Soc. Nephrol. 21: 1587-1596.
78. Iacono, A. T., B. A. Johnson, W. F. Grgurich, J. G. Youssef, T. E. Corcoran, D. A. Seiler, J. H. Dauber, G. C. Smaldone, A. Zeevi, S. A. Yousem, et al. 2006. A randomized trial of inhaled cyclosporine in lung-transplant recipients. N. Engl. J. Med. 354: 141-150.
79. Meyer, K. C. 2013. Lung transplantation. F1000Prime Rep. 5: 16.
80. Azzi, J., L. Tang, R. Moore, R. Tong, N. El Haddad, T. Akiyoshi, B. Mfarrej, S. Yang, M. Jurewicz, T. Ichimura, et al. 2010. Polylactide-cyclosporin A nanoparticles for targeted immunosuppression. FASEB J. 24: 3927-3938.
81. Tang, L., J. Azzi, M. Kwon, M. Mounayar, R. Tong, Q. Yin, R. Moore, N. Skartsis, T. M. Fan, R. Abdi, and J. Cheng. 2012. Immunosuppressive activity of size-controlled PEG-PLGA nanoparticles containing encapsulated cyclosporine A. J. Transplant. 2012: 896141.