Calcineurin inhibitors and calcineurin - NFAT system

Japanese Journal of Clinical Immunology

Volumn 33, Issue 5, 2010, Pages 249-261

  Amasaki, Yoshiharu ^a  

^a Tonan Hospital   (Japan)

Author keywords

Autoimmunity; Calcineurin; Cyclosporin A; NFAT; Tacrolimus

Indexed keywords

CALCINEURIN; CALCINEURIN INHIBITOR; CYCLOSPORIN A; TACROLIMUS; TRANSCRIPTION FACTOR NFAT;

GLUCOSE INTOLERANCE; HELPER CELL; HUMAN; IMMUNOREGULATION; LYMPHOCYTE ACTIVATION; NATURAL KILLER T CELL; NEPHROTOXICITY; REGULATORY T LYMPHOCYTE; REVIEW;

CALCINEURIN; CYCLOSPORINE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; PROTO-ONCOGENE PROTEINS C-ETS; TACROLIMUS; TRANSCRIPTION FACTOR AP-1;

EID: 78049455207     PISSN: 09114300     EISSN: 13497413     Source Type: Journal    
DOI: 10.2177/jsci.33.249     Document Type: Review

References (97)

1. Smith-Garvin JE, Koretzky GA, Jordan MS. : T cell activation. Annu Rev Immunol. 27 : 591-619, 2009.
2. 2+ store : a view from the lumen. Trends Biochem Sci. 23 : 10-14, 1998.
3. Liu JO. : Calmodulin-dependent phosphatase, kinases, and transcriptional corepressors involved in T-cell activation. Immunol Rev. 228 : 184-198, 2009.
4. Rusnak F and Mertz P : Calcineurin : form and function. Physiol Rev 80 : 1483-1521, 2000.
5. Kissinger CR, Parge HE, Knighton DR, et al. : Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature 378 : 641-644, 1995.
6. McCaffrey PG, Luo C, Kerppola TK, et al. : Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262 : 750-754, 1993.
7. Northrop JP, Ho SN, Chen L, et al. : NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369 : 497-502, 1994.
8. Hoey T, Sun YL, Williamson K, Xu X : Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2 : 461-472, 1995.
9. Masuda ES, Naito Y, Tokumitsu H, et al. : NFATx, a novel member of the nuclear factor of activated T cells family that is expressed predominantly in the thymus. Mol Cell Biol 15 : 2697-2706, 1995.
10. Ho SN, Thomas DJ, Timmerman LA, et al. : NFATc3, a lymphoid-specific NFATc family member that is calcium-regulated and exhibits distinct DNA binding specificity. J Biol Chem 270 : 19898-19907, 1995.
11. Jie L, Koyano-Nakagawa N, Amasaki Y, et al. : Calcineurin-dependent nuclear translocation of a murine transcription factor NFATx : molecular cloning and functional characterization. Mol Biol Cell 8 : 157-170, 1997.
12. Masuda ES, Liu J, Imamura R, et al. : Control of NFATx1 nuclear translocation by a calcineurin -regulated inhibitory domain. Mol Cell Biol. 17 : 2066-2075, 1997.
13. Beals CR, Clipstone NA, Ho SN, et al. : Nuclear localization of NF-ATc by a calcineurin -dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev. 11 : 824-834, 1997.
14. Luo C, Burgeon E, Carew JA, et al. : Recombinant NFAT1 (NFATp) is regulated by cal cineurin in T cells and mediates transcription of several cytokine genes. Mol. Cell. Biol. 16 : 3955-3966,1996.
15. Park J, Takeuchi A, Sharma S. : Characterization of a new isoform of the NFAT (nuclear factor of activated T cells) gene family member NFATc. J. Biol. Chem. 271 : 20914-20921, 1996.
16. Imamura R, Masuda ES, Naito Y, et al. : Carboxyl-terminal 15-amino acid sequence of NFATx1 is possibly created by tissue-specific splicing and is essential for transactivation activity in T cells. J Immunol. 161 : 3455-3463, 1998.
17. Masuda ES, Imamura R, Amasaki Y, et al. : Signalling into the T-cell nucleus : NFAT regulation. Cell Signal. 10 : 599-611, 1998.
18. Oh-hora M, Rao A. : Calcium signaling in lymphocytes. Curr Opin Immunol. 20 : 250-258, 2008.
19. Luo C, Shaw KT, Raghavan A, et al. : Interaction of calcineurin with a domain of the transcription factor NFAT1 that controls nuclear import. Proc Natl Acad Sci USA. 93 : 8907-8912, 1996.
20. Liu J, Arai K, Arai N. : Inhibition of NFATx activation by an oligopeptide : disrupting the interaction of NFATx with calcineurin. J Immunol. 167 : 2677-2687, 2001.
21. Shibasaki F, Price ER, Milan D, et al. : Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382 : 370-373, 1996.
22. Beals CR, Sheridan CM, Turck CW, et al. : Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science. 275 : 1930-1934, 1997.
23. Okamura H, Garcia-Rodriguez C, Martinson H, et al. : A conserved docking motif for CK1 binding controls the nuclear localization of NFAT1. Mol Cell Biol. 24 : 4184-4195, 2004.
24. Arron JR, Winslow MM, Polleri A, et al. : NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature. 441 : 595-600, 2006.
25. Gwack Y, Sharma S, Nardone J, et al. : A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature. 441 : 646-650, 2006.
26. Miyakawa H, Woo SK, Dahl SC, et al. : Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc Natl Acad Sci USA. 96 : 2538-2542, 1999.
27. Lopez-Rodríguez C, Aramburu J, Rakeman AS, et al. : NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc Natl Acad Sci USA. 96. 7214-7219, 1999.
28. Pan S, Tsuruta R, Masuda ES, et al. : NFATz : a novel rel similarity domain containing protein. Biochem Biophys Res Commun. 272 : 765-776, 2000.
29. López-Rodríguez C, Aramburu J, Jin L, et al. : Bridging the NFAT and NF-kappaB families : NFAT5 dimerization regulates cytokine gene transcription in response to osmotic stress. Immunity. 15 : 47-58, 2001.
30. Graef IA, Gastier JM, Francke U, et al. : Evolutionary relationships among Rel domains indicate functional diversification by recombination. Proc Natl Acad Sci USA. 98, 5740-5745, 2001.
31. Wu H, Peisley A, Graef IA, et al. : NFAT signaling and the invention of vertebrates. Trends Cell Biol. 17 : 251-260, 2007.
32. Zhou P, Sun LJ, Dötsch V, Wagner G, Verdine GL. : Solution structure of the core NFATC1/DNA complex. Cell 92 : 687-696, 1998.
33. Chinenov Y, Kerppola TK : Close encounters of many kinds : Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene. 20 : 2438-2452, 2001.
34. de Grazia U, Felli MP, Vacca A, et al. : Positive and negative regulation of the composite octamer motif of the interleukin 2 enhancer by AP-1, Oct-2, and retinoic acid receptor. J Exp Med. 180 : 1485-1497, 1994.
35. Boise LH, Petryniak B, Mao X, et al. : The NFAT-1 DNA binding complex in activated T cells contains Fra-1 and JunB. Mol Cell Biol. 13 : 1911-1919, 1993.
36. Chen L, Glover JN, Hogan PG, et al. : Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature. 392 : 42-48, 1998.
37. Josefowicz SZ, Rudensky A. : Control of regulatory T cell lineage commitment and maintenance. Immunity 30 : 616-625, 2009.
38. Wildin RS, Ramsdell F, Peake J, et al. : X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet. 27 : 18-20, 2001.
39. Bennett CL, Christie J, Ramsdell F, et al. : The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet. 27 : 20-21, 2001.
40. Wu Y, Borde M, Heissmeyer V, et al. : FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell. 126 : 375-387, 2006.
41. Bandukwala H, Wu Y, Feeirer M, et al. : Structure of a domain-swapped FOXP3 dimer on DNA and its function in regulatory T cells. Int Immunol 22 suppl. 1 (SY4-4-1), 2010.
42. Ruan Q, Kameswaran V, Tone Y, et al. : Development of Foxp3(+) regulatory t cells is driven by the c-Rel enhanceosome. Immunity. 31 : 932-940, 2009.
43. + T cells. Curr. Opin. Immunol. 8 : 225-232, 1996.
44. Singer A, Adoro S, Park JH. : Lineage fate and intense debate : myths, models and mechanisms of CD4- versus CD8-lineage choice. Nat Rev Immunol. 8 : 788-801, 2008.
45. + thymocytes. J. Immunol. 144 : 3611-3618, 1990.
46. Fischer M, MacNeil I, Suda T, et al. : Cytokine production by mature and immature thymocytes. J. Immunol. 146 : 3452-3456, 1991.
47. Swan KA, Alberola-Ila J, Gross JA, et al. : Involvement of p21ras distinguishes positive and negative selection in thymocytes. EMBO J. 14 : 276-285, 1995.
48. Alberola-Ila J, Hogquist KA, Swan KA, et al. : Positive and negative selection invoke distinct signaling pathways. J Exp Med. Jul 184 : 9-18, 1996.
49. Bueno OF, Brandt EB, Rothenberg ME, et al. : Defective T cell development and function in calcineurin A beta -deficient mice. Proc Natl Acad Sci USA. 99 : 9398-9403, 2002.
50. Gallo EM, Winslow MM, Canté-Barrett K, et al. : Calcineurin sets the bandwidth for discrimination of signals during thymocyte development. Nature. 450 : 731-735, 2007.
51. Amasaki Y, Masuda ES, Imamura R, et al. : Distinct NFAT family proteins are involved in the nuclear NFAT-DNA binding complexes from human thymocyte subsets. J Immunol. 160 : 2324-2333, 1998.
52. Oukka M, Ho IC, de la Brousse FC, et al. : The transcription factor NFAT4 is involved in the generation and survival of T cells. Immunity 9 : 295-304, 1998.
53. + T cells. J Biol Chem. 277 : 25640-25648, 2002.
54. Gallo EM, Winslow MM, Cant?-Barrett K, et al. : Calcineurin sets the bandwidth for discrimination of signals during thymocyte development. Nature. 450 : 731-735, 2007.
55. Lazarevic V, Zullo AJ, Schweitzer MN, et al. : The gene encoding early growth response 2, a target of the transcription factor NFAT, is required for the development and maturation of natural killer T cells. Nat Immunol. 10 : 306-313, 2009.
56. Rengarajan J, Mittelstadt PR, Mages HW, Gerth AJ, Kroczek RA, Ashwell JD, Glimcher LH. : Sequential involvement of NFAT and Egr transcription factors in FasL regulation. Immunity 12 : 293-300, 2000.
57. + distinguished in the early growth response (Egr)-1 transgenic mice with a recombinase -activating gene-deficient background. J Exp Med. 186 : 877-885, 1997.
58. + stage. J Immunol. 168 : 1649-1658, 2002.
59. Carter JH, Lefebvre JM, Wiest DL, et al. : Redundant role for early growth response transcriptional regulators in thymocyte differentiation and survival. J Immunol. 178 : 6796-6805, 2007.
60. Safford M, Collins S, Lutz MA, et al. : Egr-2 and Egr-3 are negative regulators of T cell activation. Nat Immunol. 6 : 472-480, 2005.
61. Xanthoudakis S, Viola JP, Shaw KT, et al. : An enhanced immune response in mice lacking the transcription factor NFAT1. Science. 272 : 892-895, 1996.
62. Yoshida H, Nishina H, Takimoto H, et al. : The transcription factor NF-ATc1 regulate lymphocyte proliferation and Th2 cytokine production. Immunity 8 : 115-124, 1998.
63. Ranger AM, Hodge MR, Gravallese EM, et al. : Delayed lymphoid repopulation with defects in IL-4-driven responses produced by inactivation of NF-ATc. Immunity 8 : 125-134, 1998.
64. Peng SL, Gerth AJ, Ranger AM, et al.: NFATc1 and NFATc2 together control both T and B cell activation and differentiation. Immunity 14 : 13-20, 2001.
65. Ranger AM, Oukka M, Rengarajan J, et al. : Inhibitory function of two NFAT family members n lymphoid homeostasis and Th2 development. Immunity 9 : 627-635, 1998.
66. Bopp T, Palmetshofer A, Serfling E, et al. : NFATc2 and NFATc3 transcription factors play a crucial role in suppression of CD4+ T lymphocytes by CD4+ CD25+ regulatory T cells. J Exp Med. 201 : 181-187, 2005.
67. + T cells. J Immunol. 170 : 3109-3117, 2003.
68. Molkentin JD, Lu JR, Antos CL, et al. : A calcineurin -dependent transcriptional pathway for cardiac hypertrophy. Cell 93 : 215-228, 1998.
69. de la Pompa JL, Timmerman LA, Takimoto H, et al. : Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature. 392 : 182-186, 1998.
70. Saneyoshi T, Kume S, Amasaki Y, et al. : The Wnt/calcium pathway activates NF-AT and promotes ventral cell fate in Xenopus embryos. Nature 417 : 295-299, 2002.
71. Takayanagi H, Kim S, Koga T, et al. : Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell. 3 : 889-901, 2002.
72. Liu J, Farmer JD Jr, Lane WS, et al. : Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell. 66 : 807-815, 1991.
73. Gä othel SF, Marahiel MA. : Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci. 55 : 423-436, 1999.
74. Huai Q, Kim HY, Liu Y, et al. : Crystal structure of calcineurin- cyclophilin-cyclosporin shows common but distinct recognition of immunophilin-drug complexes. Proc Natl Acad Sci USA. 99 : 12037-12042, 2002.
75. Gallo EM, Ho L, Winslow MM, et al. : Selective role of calcineurin in haematopoiesis and lymphopoiesis. EMBO Rep. 9 : 1141-1148, 2008.
76. Lee YH, Lee YR, Im SA, et al. : Calcineurin inhibitors block MHC-restricted antigen presentation in vivo. J Immunol. 179 : 5711-5716, 2007.
77. Bansal T, Jaggi M, Khar RK, et al. : Emerging significance of flavonoids as P-glycoprotein inhibitors in cancer chemotherapy. J Pharm Pharm Sci. 12 : 46-78, 2009.
78. Hesselink DA, van Schaik RH, van der Heiden IP, et al. : Genetic polymorphisms of the CYP3A4, CYP3A5, and MDR-1 genes and pharmacokinetics of the calcineurin inhibitors cyclosporine and tacrolimus. Clin Pharmacol Ther. 74 : 245-254, 2003.
79. Andoh TF, Burdmann EA, Bennett WM. : Nephrotoxicity of immunosuppressive drugs : experimental and clinical observations. Semin Nephrol. 17 : 34-45, 1997.
80. Böttiger Y, Brattström C, Tydén G, et al. : Tacrolimus whole blood concentrations correlate closely to side-effects in renal transplant recipients. Br J Clin Pharmacol. 48 : 445-448, 1999.
81. Tamura K, Fujimura T, Tsutsumi T, et al. : Transcriptional inhibition of insulin by FK506 and possible involvement of FK506 binding protein-12 in pancreatic beta-cell. Transplantation 59 : 1606-1613, 1995.
82. Davies TH, Ning YM, Sánchez ER. : Differential control of glucocorticoid receptor hormone-binding function by tetratricopeptide repeat (TPR) proteins and the immunosuppressive ligand FK506. Biochemistry. 44 : 2030-2038, 2005.
83. Hutchinson IV, Bagnall W, Bryce P, et al. : Differences in the mode of action of cyclosporine and FK 506. Transplant Proc. 30 : 959-960, 1998.
84. Hultsch T, Kapp A, Spergel J. : Immunomodulation and safety of topical calcineurin inhibitors for the treatment of atopic dermatitis. Dermatolog 211 : 174-187, 2005. (Pubitemid 41160263)
85. Lampropoulos CE, D'Cruz DP. : Topical calcineurin inhibitors in systemic lupus erythematosus. Ther Clin Risk Manag. 6 : 95-101, 2010.
86. Cunningham MA, Austin BA, Li Z, et al. : LX211 (voclosporin) suppresses experimental uveitis and inhibits human T cells. Invest Ophthalmol Vis Sci. 50 : 249-255, 2009.
87. Papp K, Bissonnette R, Rosoph L, et al. : Efficacy of ISA247 in plaque psoriasis : a randomised, multicentre, double-blind, placebo-controlled phase III study. Lancet 371 : 1337-1342, 2008.
88. Gaber AO, Busque S, Mulgaonkar S, et al. : ISA247 : A phase IIB multicenter, open label, concentration-controlled trial in de novo renal transplantation. Am J Transplant 8(Suppl 2): 336, 2008.
89. Cooper JE, Wiseman AC. : Novel immunosuppressive agents in kidney transplantation. Clin Nephrol. 73 : 333-343, 2010.
90. Torgerson TR, Colosia AD, Donahue JP, et al. : Regulation of NF-kappa B, AP-1, NFAT, and STAT1 nuclear import in T lymphocytes by noninvasive delivery of peptide carrying the nuclear localization sequence of NF-kappa B p50. J Immunol. 161 : 6084-6092, 1998.
91. Tomita T, Takeuchi E, Tomita N, et al. : Suppressed severity of collagen-induced arthritis by in vivo transfection of nuclear factor kappaB decoy oligodeoxynucleotides as a gene therapy. Arthritis Rheum. 42 : 2532-2342, 1999.
92. Aramburu J, Yaffe MB, López-Rodríguez C, et al. : Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285 : 2129-2133, 1999.
93. Noguchi H, Matsushita M, Okitsu T, et al. : A new cell-permeable peptide allows successful allogeneic islet transplantation in mice. Nat Med. 10 : 305-309, 2004.
94. Yu H, van Berkel TJ, Biessen EA. : Therapeutic potential of VIVIT, a selective peptide inhibitor of nuclear factor of activated T cells, in cardiovascular disorders. Cardiovasc Drug Rev. 25 : 175-187, 2007.
95. Huang GN, Huso DL, Bouyain S, et al. : NFAT binding and regulation of T cell activation by the cytoplasmic scaffolding Homer proteins. Science 319 : 476-481, 2008.