Interaction of calcineurin with substrates and targeting proteins

Trends in Cell Biology

Volumn 21, Issue 2, 2011, Pages 91-103

  Li, Huiming ^a,b   Rao, Anjana ^a,b,c   Hogan, Patrick G ^a,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

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

CALCIUM SIGNALING; CALCIUM TRANSPORT; DEVELOPMENTAL DISORDER; DOWN SYNDROME; DRUG PROTEIN BINDING; DRUG TARGETING; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCINEURIN; CALCIUM; HUMANS; IMMUNOSUPPRESSIVE AGENTS; NFATC TRANSCRIPTION FACTORS; SIGNAL TRANSDUCTION;

EID: 79151468994     PISSN: 09628924     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tcb.2010.09.011     Document Type: Review

References (120)

1. Roy J., Cyert M.S. Cracking the phosphatase code: docking interactions determine substrate specificity. Sci. Signal. 2009, 2. re9, 1-7.
2. Shi Y. Serine/threonine phosphatases: mechanism through structure. Cell 2009, 139:468-484.
3. Aramburu J., et al. Calcineurin: from structure to function. Curr. Top. Cell Regul. 2000, 36:237-295.
4. Rusnak F., Mertz P. Calcineurin: form and function. Physiol. Rev. 2000, 80:1483-1521.
5. Griffith J.P., et al. X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell 1995, 82:507-522.
6. Kissinger C.R., et al. Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature 1995, 378:641-644.
7. Gallagher S.C., et al. There is communication between all four Ca(2+)-binding sites of calcineurin B. Biochemistry 2001, 40:12094-12102.
8. Kakalis L.T., et al. Characterization of the calcium-binding sites of calcineurin B. FEBS Lett. 1995, 362:55-58.
9. Klee C.B., et al. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J. Biol. Chem. 1998, 273:13367-13370.
10. Stemmer P.M., Klee C.B. Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 1994, 33:6859-6866.
11. Yang S.A., Klee C.B. Low affinity Ca2+-binding sites of calcineurin B mediate conformational changes in calcineurin A. Biochemistry 2000, 39:16147-16154.
12. Shen X., et al. The secondary structure of calcineurin regulatory region and conformational change induced by calcium/calmodulin binding. J. Biol. Chem. 2008, 283:11407-11413.
13. Wang H., et al. A renewed model of CNA regulation involving its C-terminal regulatory domain and CaM. Biochemistry 2008, 47:4461-4468.
14. Huai Q., et al. Crystal structure of calcineurin-cyclophilin-cyclosporin shows common but distinct recognition of immunophilin-drug complexes. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:12037-12042.
15. Jin L., Harrison S.C. Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13522-13526.
16. Liu J., et al. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 1991, 66:807-815.
17. Shaw K.T., et al. Immunosuppressive drugs prevent a rapid dephosphorylation of transcription factor NFAT1 in stimulated immune cells. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:11205-11209.
18. Cahalan M.D. STIMulating store-operated Ca(2+) entry. Nat. Cell Biol. 2009, 11:669-677.
19. Hogan P.G., et al. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 2010, 28:491-533.
20. Gwack Y., et al. A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 2006, 441:646-650.
21. Arron J.R., et al. NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature 2006, 441:595-600.
22. Okamura H., et al. A conserved docking motif for CK1 binding controls the nuclear localization of NFAT1. Mol. Cell Biol. 2004, 24:4184-4195.
23. Heineke J., Molkentin J.D. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat. Rev. Mol. Cell Biol. 2006, 7:589-600.
24. Molkentin J.D., et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 1998, 93:215-228.
25. Serfling E., et al. NFAT transcription factors in control of peripheral T cell tolerance. Eur. J. Immunol. 2006, 36:2837-2843.
26. Sundrud M.S., Rao A. New twists of T cell fate: control of T cell activation and tolerance by TGF-beta and NFAT. Curr. Opin. Immunol. 2007, 19:287-293.
27. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat. Rev. Immunol. 2007, 7:292-304.
28. Yamin G. NMDA receptor-dependent signaling pathways that underlie amyloid beta-protein disruption of LTP in the hippocampus. J. Neurosci. Res. 2009, 87:1729-1736.
29. Berridge M.J. Calcium hypothesis of Alzheimer's disease. Pflugers Arch. 2010, 459:441-449.
30. Ryeom S., et al. Targeted deletion of the calcineurin inhibitor DSCR1 suppresses tumor growth. Cancer Cell 2008, 13:420-431.
31. Mancini M., Toker A. NFAT proteins: emerging roles in cancer progression. Nat. Rev. Cancer 2009, 9:810-820.
32. Baek K.H., et al. Down's syndrome suppression of tumour growth and the role of the calcineurin inhibitor DSCR1. Nature 2009, 459:1126-1130.
33. Aramburu J., et al. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT. Mol. Cell 1998, 1:627-637.
34. Garcia-Cozar F.J., et al. Two-site interaction of nuclear factor of activated T cells with activated calcineurin. J. Biol. Chem. 1998, 273:23877-23883.
35. Aramburu J., et al. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 1999, 285:2129-2133.
36. Li H., et al. Structure of calcineurin in complex with PVIVIT peptide: portrait of a low-affinity signalling interaction. J. Mol. Biol. 2007, 369:1296-1306.
37. Li H., et al. Structural delineation of the calcineurin-NFAT interaction and its parallels to PP1 targeting interactions. J. Mol. Biol. 2004, 342:1659-1674.
38. Ye Q., et al. The complex structure of calmodulin bound to a calcineurin peptide. Proteins 2008, 73:19-27.
39. Majava V., Kursula P. Domain swapping and different oligomeric States for the complex between calmodulin and the calmodulin-binding domain of calcineurin a. PLoS One 2009, 4:e5402.
40. Liu J., et al. Inhibition of NFATx activation by an oligopeptide: disrupting the interaction of NFATx with calcineurin. J. Immunol. 2001, 167:2677-2687.
41. Liu J., et al. Two independent calcineurin-binding regions in the N-terminal domain of murine NF-ATx1 recruit calcineurin to murine NF-ATx1. J. Immunol. 1999, 162:4755-4761.
42. Park S., et al. A second calcineurin binding site on the NFAT regulatory domain. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7130-7135.
43. Dougherty M.K., et al. KSR2 is a calcineurin substrate that promotes ERK cascade activation in response to calcium signals. Mol. Cell 2009, 34:652-662.
44. Rodriguez A., et al. A conserved docking surface on calcineurin mediates interaction with substrates and immunosuppressants. Mol. Cell 2009, 33:616-626.
45. Martinez-Martinez S., et al. Blockade of NFAT activation by the second calcineurin binding site. J. Biol. Chem. 2006, 281:6227-6235.
46. Mehta S., et al. Domain architecture of the regulators of calcineurin (RCANs) and identification of a divergent RCAN in yeast. Mol. Cell Biol. 2009, 29:2777-2793.
47. Roy J., et al. A conserved docking site modulates substrate affinity for calcineurin, signaling output, and in vivo function. Mol. Cell 2007, 25:889-901.
48. Wiedemann U., et al. Quantification of PDZ domain specificity, prediction of ligand affinity and rational design of super-binding peptides. J. Mol. Biol. 2004, 343:703-718.
49. Muller M.R., et al. Requirement for balanced Ca/NFAT signaling in hematopoietic and embryonic development. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7034-7039.
50. Cyert M.S. Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem. Biophys. Res. Commun. 2003, 311:1143-1150.
51. Boustany L.M., Cyert M.S. Calcineurin-dependent regulation of Crz1p nuclear export requires Msn5p and a conserved calcineurin docking site. Genes Dev. 2002, 16:608-619.
52. Heath V.L., et al. Hph1p and Hph2p, novel components of calcineurin-mediated stress responses in Saccharomyces cerevisiae. Eukaryot. Cell 2004, 3:695-704.
53. Bultynck G., et al. Slm1 and slm2 are novel substrates of the calcineurin phosphatase required for heat stress-induced endocytosis of the yeast uracil permease. Mol. Cell Biol. 2006, 26:4729-4745.
54. Cohen P.T. Protein phosphatase 1-targeted in many directions. J. Cell Sci. 2002, 115:241-256.
55. Bollen M., et al. The extended PP1 toolkit: designed to create specificity. Trends Biochem. Sci. 2010, 35:450-458.
56. Sano Y., et al. A novel two-pore domain K+ channel, TRESK, is localized in the spinal cord. J. Biol. Chem. 2003, 278:27406-27412.
57. Czirjak G., et al. The two-pore domain K+ channel, TRESK, is activated by the cytoplasmic calcium signal through calcineurin. J. Biol. Chem. 2004, 279:18550-18558.
58. Dobler T., et al. TRESK two-pore-domain K+ channels constitute a significant component of background potassium currents in murine dorsal root ganglion neurones. J. Physiol. 2007, 585:867-879.
59. Kang D., Kim D. TREK-2 (K2P10.1) and TRESK (K2P18.1) are major background K+ channels in dorsal root ganglion neurons. Am. J. Physiol. Cell Physiol. 2006, 291:C138-146.
60. Smith H.S. Calcineurin as a nociceptor modulator. Pain Physician 2009, 12:E309-318.
61. Czirjak G., Enyedi P. Targeting of calcineurin to an NFAT-like docking site is required for the calcium-dependent activation of the background K+ channel, TRESK. J. Biol. Chem. 2006, 281:14677-14682.
62. Kolch W. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 2005, 6:827-837.
63. McKay M.M., Morrison D.K. Integrating signals from RTKs to ERK/MAPK. Oncogene 2007, 26:3113-3121.
64. Ory S., et al. Protein phosphatase 2A positively regulates Ras signaling by dephosphorylating KSR1 and Raf-1 on critical 14-3-3 binding sites. Curr. Biol. 2003, 13:1356-1364.
65. Oliveria S.F., et al. AKAP79/150 anchoring of calcineurin controls neuronal L-type Ca2+ channel activity and nuclear signaling. Neuron 2007, 55:261-275.
66. Taigen T., et al. Targeted inhibition of calcineurin prevents agonist-induced cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1196-1201.
67. Dell'Acqua M.L., et al. Mapping the protein phosphatase-2B anchoring site on AKAP79. Binding and inhibition of phosphatase activity are mediated by residues 315-360. J. Biol. Chem. 2002, 277:48796-48802.
68. Coghlan V.M., et al. Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 1995, 267:108-111.
69. Lai M.M., et al. Cain, a novel physiologic protein inhibitor of calcineurin. J. Biol. Chem. 1998, 273:18325-18331.
70. Dell'Acqua M.L., et al. Regulation of neuronal PKA signaling through AKAP targeting dynamics. Eur. J. Cell Biol. 2006, 85:627-633.
71. Bhattacharyya S., et al. A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors. Nat. Neurosci. 2009, 12:172-181.
72. Snyder E.M., et al. Role for A kinase-anchoring proteins (AKAPS) in glutamate receptor trafficking and long term synaptic depression. J. Biol. Chem. 2005, 280:16962-16968.
73. Jurado S., et al. A calcineurin/AKAP complex is required for NMDA receptor-dependent long-term depression. Nat. Neurosci. 2010, 13:1053-1055.
74. Lee H.K., et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 2003, 112:631-643.
75. Whitlock J.R., et al. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
76. Tavalin S.J., et al. Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J. Neurosci. 2002, 22:3044-3051.
77. Davies K.J., et al. Renaming the DSCR1/Adapt78 gene family as RCAN: regulators of calcineurin. Faseb. J. 2007, 21:3023-3028.
78. Gorlach J., et al. Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans. EMBO. J. 2000, 19:3618-3629.
79. Kingsbury T.J., Cunningham K.W. A conserved family of calcineurin regulators. Genes Dev. 2000, 14:1595-1604.
80. Fuentes J.J., et al. Genomic organization, alternative splicing, and expression patterns of the DSCR1 (Down syndrome candidate region 1) gene. Genomics 1997, 44:358-361.
81. Ermak G., et al. Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer's disease. J. Biol.Chem. 2001, 276:38787-38794.
82. Fuentes J.J., et al. DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways. Hum. Mol. Genet. 2000, 9:1681-1690.
83. Chan B., et al. Identification of a peptide fragment of DSCR1 that competitively inhibits calcineurin activity in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13075-13080.
84. Rothermel B., et al. A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling. J. Biol. Chem. 2000, 275:8719-8725.
85. Ermak G., et al. The DSCR1 (Adapt78) isoform 1 protein calcipressin 1 inhibits calcineurin and protects against acute calcium-mediated stress damage, including transient oxidative stress. FASEB. J. 2002, 16:814-824.
86. Rothermel B.A., et al. Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3328-3333.
87. Ryeom S., et al. The threshold pattern of calcineurin-dependent gene expression is altered by loss of the endogenous inhibitor calcipressin. Nat. Immunol. 2003, 4:874-881.
88. Yang J., et al. Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ. Res. 2000, 87:E61-68.
89. Hilioti Z., et al. GSK-3 kinases enhance calcineurin signaling by phosphorylation of RCNs. Genes Dev. 2004, 18:35-47.
90. Hilioti Z., Cunningham K.W. The RCN family of calcineurin regulators. Biochem. Biophys. Res. Commun. 2003, 311:1089-1093.
91. Vega R.B., et al. Dual roles of modulatory calcineurin-interacting protein 1 in cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:669-674.
92. Liu Q., et al. Interaction between TAK1-TAB1-TAB2 and RCAN1-calcineurin defines a signalling nodal control point. Nat. Cell Biol. 2009, 11:154-161.
93. Sanna B., et al. Modulatory calcineurin-interacting proteins 1 and 2 function as calcineurin facilitators in vivo. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:7327-7332.
94. Vega R.B., et al. Multiple domains of MCIP1 contribute to inhibition of calcineurin activity. J. Biol. Chem. 2002, 277:30401-30407.
95. Abbasi S., et al. Protein kinase-mediated regulation of calcineurin through the phosphorylation of modulatory calcineurin-interacting protein 1. J. Biol. Chem. 2006, 281:7717-7726.
96. Kishi T., et al. The SCFCdc4 ubiquitin ligase regulates calcineurin signaling through degradation of phosphorylated Rcn1, an inhibitor of calcineurin. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17418-17423.
97. Martinez-Martinez S., et al. The RCAN carboxyl end mediates calcineurin docking-dependent inhibition via a site that dictates binding to substrates and regulators. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6117-6122.
98. Mulero M.C., et al. Inhibiting the calcineurin-NFAT (nuclear factor of activated T cells) signaling pathway with a regulator of calcineurin-derived peptide without affecting general calcineurin phosphatase activity. J. Biol. Chem. 2009, 284:9394-9401.
99. Wang J.H., Desai R. Modulator binding protein. Bovine brain protein exhibiting the Ca2+-dependent association with the protein modulator of cyclic nucleotide phosphodiesterase. J. Biol. Chem. 1977, 252:4175-4184.
100. Klee C.B., Krinks M.H. Purification of cyclic 3′,5′-nucleotide phosphodiesterase inhibitory protein by affinity chromatography on activator protein coupled to Sepharose. Biochemistry 1978, 17:120-126.
101. Fruman D.A., et al. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporin A. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:3686-3690.
102. Swanson S.K., et al. Cyclosporin-mediated inhibition of bovine calcineurin by cyclophilins A and B. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:3741-3745.
103. McCaffrey P.G., et al. Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 1993, 262:750-754.
104. Northrop J.P., et al. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 1994, 369:497-502.
105. Pettersen E.F., et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
106. DeLano, W.L. (2002) The PyMOL Molecular Graphics System, Version 1.3, Schrödinger LLC.
107. Jain J., et al. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 1993, 365:352-355.
108. Mochida S., Hunt T. Calcineurin is required to release Xenopus egg extracts from meiotic M phase. Nature 2007, 449:336-340.
109. Nishiyama T., et al. Transient activation of calcineurin is essential to initiate embryonic development in Xenopus laevis. Nature 2007, 449:341-345.
110. Ingebritsen T.S., Cohen P. The protein phosphatases involved in cellular regulation. 1. Classification and substrate specificities. Eur. J. Biochem. 1983, 132:255-261.
111. Mao Z., Wiedmann M. Calcineurin enhances MEF2 DNA binding activity in calcium-dependent survival of cerebellar granule neurons. J. Biol. Chem. 1999, 274:31102-31107.
112. Wang H.G., et al. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999, 284:339-343.
113. Stathopoulos A.M., Cyert M.S. Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev. 1997, 11:3432-3444.
114. Matheos D.P., et al. Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes Dev. 1997, 11:3445-3458.
115. Cribbs J.T., Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 2007, 8:939-944.
116. Liu Y.V., et al. Calcineurin promotes hypoxia-inducible factor 1alpha expression by dephosphorylating RACK1 and blocking RACK1 dimerization. J. Biol. Chem. 2007, 282:37064-37073.
117. Lieberman D.N., Mody I. Regulation of NMDA channel function by endogenous Ca(2+)-dependent phosphatase. Nature 1994, 369:235-239.
118. Goto S., et al. Dephosphorylation of microtubule-associated protein 2, tau factor, and tubulin by calcineurin. J. Neurochem. 1985, 45:276-283.
119. Wang Y., et al. Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J. Biol. Chem. 2005, 280:12683-12689.
120. Li J., et al. The mAKAPβ scaffold regulates cardiac myocyte hypertrophy via recruitment of activated calcineurin. J. Mol. Cell. Cardiol. 2010, 48:387-394.