Immunophilins in the nervous system

Neuron

Volumn 21, Issue 2, 1998, Pages 283-294

  Snyder, Solomon H ^a   Lai, Michael M ^a   Burnett, Patrick E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (3,3 DIMETHYL 1,2 DIOXOPENTYL) 2 PYRROLIDINECARBOXYLIC ACID 3 (3 PYRIDYL)PROPYL ESTER; CALCINEURIN; CYCLOSPORIN A; FK 506 BINDING PROTEIN; IMMUNOPHILIN; IMMUNOSUPPRESSIVE AGENT; INOSITOL 1,4,5 TRISPHOSPHATE; RAPAMYCIN; RYANODINE; TACROLIMUS; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG;

BRAIN PROTECTION; DRUG MECHANISM; DRUG RECEPTOR BINDING; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; NERVE REGENERATION; NERVOUS SYSTEM; NEUROTOXICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; STROKE;

EID: 0032142911     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80538-3     Document Type: Review

References (107)

1. Abe, K., Chu, P.J., Ishihara, A., and Saito, H. (1996). Transforming growth factor-beta 1 promotes re-elongation of injured axons of cultured rat hippocampal neurons. Brain Res. 732, 206-209.
2. Atkison, P., Joubert, G., Barron, A., Grant, D., Paradis, K., Seidman, E., Wall, W., Rosenberg, H., Howard, J., Williams, S., et al. (1995). Hypertrophic cardiomyopathy associated with tacrolimus in paediatric transplant patients. Lancet 345, 894-896.
3. Basi, G.S., Jacobson, R.D., Virag, I., Schilling, J., and Skene, J.H.P. (1987). Primary structure and transcriptional regulation of GAP-43, a protein associated with nerve growth. Cell 49, 785-791.
4. Baughman, G., Wiederrecht, G.J., Campbell, N.F., Martin, M.M., and Bourgeois, S. (1995). FKBP51, a novel T-cell-specific immunophilin capable of calcineurin inhibition. Mol. Cell. Biol. 15, 4395-4402.
5. Beretta, L., Gingras, A.C., Svitkin, Y.V., Hall, M.N., and Sonenberg, N. (1996). Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 15, 658-664.
6. Betz, H., Kuhse, J., Fischer, M., Schmieden, V., Laube, B., Kuryatov, A., Langosch, D., Meyer, G., Bormann, J., Rundstrom, N., et al. (1994). Structure, diversity and synaptic localization of inhibitory glycine receptors. J. Physiol. (Paris) 88, 243-248.
7. Bierer, B.E., Mattila, P.S., Standaert, R.F., Herzenberg, L.A., Burakoff, S.J., Crabtree, G., and Schreiber, S.L. (1990a). Two distinct signal transmission pathways in T lymphocytes are inhibited by complexes formed between an immunophilin and either FK506 or rapamycin. Proc. Natl. Acad. Sci. USA 87, 9231-9235.
8. Bierer, B.E., Somers, P.K., Wandless, T.J., Burakoff, S.J., and Schreiber, S.L. (1990b). Probing immunosuppressant action with a nonnatural immunophilin ligand. Science 250, 556-559.
9. Bierer, B.E., Jin, Y.J., Fruman, D.A., Calvo, V., and Burakoff, S.J. (1991). FK 506 and rapamycin: molecular probes of T-lymphocyte activation. Transplant. Proc. 23, 2850-2855.
10. Borel, J.F., Feurer, C., Gubler, H.U., and Steahelin, H. (1976). Biological effects of cyclosporine A: a new antilymphocytic agent. Agents Actions Suppl. 6, 468-475.
11. Bredt, D.S., Ferris, C.D., and Snyder, S.H. (1992). Nitric oxide synthase regulatory sites. Phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J. Biol. Chem. 267, 10976-10981.
12. Brillantes, A.B., Ondrias, K., Scott, A., Kobrinsky, E., Ondriasova, E., Moschella, M.C., Jayaraman, T., Landers, M., Ehrlich, B.E., and Marks, A.R. (1994). Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513-523.
13. Brown, E.J., Albers, M.W., Shin, T.B., Ichikawa, K., Keith, C.T., Lane, W.S., and Schreiber, S.L. (1994). A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 369, 756-758.
14. Brunn, G.J., Hudson, C.C., Sekulic, A., Williams, J.M., Hosoi, H., Houghton, P.J., Lawrence, J.C.J., and Abraham, R.T. (1997). Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277, 99-101.
15. Burnett, P.E., Barrow, R.K., Cohen, N.A., Snyder, S.H., and Sabatini, D.M. (1998a). RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. USA 95, 1432-1437.
16. Burnett, P.E., Blackshaw, S., Lai, M.M., Qureshi, I.A., Burnett, A.F., Sabatini, D.M., and Snyder, S.H. (1998b). Neurabin is a synaptic protein linking p70 S6 kinase and the neuronal cytoskeleton. Proc. Natl. Acad. Sci. USA 95, 8351-8356.
17. Butcher, S.P., Henshall, D.C., Teramura, Y., Iwasaki, K., and Sharkey, J. (1997). Neuroprotective actions of FK506 in experimental stroke: in vivo evidence against an antiexcitotoxic mechanism. J. Neurosci. 17, 6939-6946.
18. Cameron, A.M., Steiner, J.P., Sabatini, D.M., Kaplin, A.I., Walensky, L.D., and Snyder, S.H. (1995a). Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Sci. USA 92, 1784-1788.
19. 2+ flux. Cell 83, 463-472.
20. Cameron, A.M., Nucifora, F.C., Fung, E.T., Livingston, D.J., Aldape, R.A., Ross, C.A., and Snyder, S.H. (1997). FKBP12 binds the inositol 1,4,5-triphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. J. Biol. Chem. 272, 27582-27588.
21. Cardenas, M.E., and Heitman, J. (1995). FKBP12-rapamycin target TOR2 is a vacuolar protein with an associated phosphatidylinositol-4 kinase activity. EMBO J. 14, 5892-5907.
22. Chambraud, B., Radanyi, C., Camonis, J.H., Shazand, K., Rajkowski, K., and Baulieu, E.E. (1996). FAP48, a new protein that forms specific complexes with both immunophilins FKBP59 and FKBP12. Prevention by the immunosuppressant drugs FK506 and rapamycin. J. Biol. Chem. 271, 32923-32929.
23. Charng, M.J., Kinnunen, P., Hawker, J., Brand, T., and Schneider, M.D. (1996). FKBP-12 recognition is dispensable for signal generation by type I transforming growth factor-beta receptors. J. Biol. Chem. 277, 22941-22944.
24. Chen, H., Wu, J., Xu, D., Luo, H., and Daloze, P. (1992). Efficacy and mechanism of action of rapamycin in presensitized recipients of experimental allografts. Transplant. Proc. 24, 1669-1670.
25. Chen, Y.G., Liu, F., and Massagué, J. (1997). Mechanism of TGFβ receptor inhibition by FKBP12. EMBO J. 16, 3866-3876.
26. Chiu, M.I., Katz, H., and Berlin, V. (1994). RAPT1, a mammalian homolog of yeast Tor, interacts with the FKBP12/rapamycin complex. Proc. Natl. Acad. Sci. USA 91, 12574-12578.
27. Choi, D.W. (1988). Glutamate neurotoxicity in diseases of the nervous system. Neuron 1, 623-624.
28. Chung, J., Kuo, C.J., Crabtree, G.R., and Blenis, J. (1992). Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases. Cell 69, 1227-1236.
29. Coghlan, V.M., Perrino, B.A., Howard, M., Langeberg, L.K., Hicks, J.B., Gallatin, W.M., and Scott, J.D. (1995). Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 267, 108-111.
30. Dawson, T.M., Steiner, J.P., Dawson, V.L., Dinerman, J.L., Uhl, G.R., and Snyder, S.H. (1993). Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc. Natl. Acad. Sci. USA 90, 9808-9812.
31. Dawson, T.M., Steiner, J.P., Lyons, W.E., Fotuhi, M., Blue, M., and Snyder, S.H. (1994). The immunophilins, FK506 binding protein and cyclophilin, are discretely localized in the brain: relationship to calcineurin. Neuroscience 62, 569-580.
32. De Camilli, P., and Takei, K. (1996). Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16, 2479-2487.
33. Dumont, F.J., Melino, M.R., Staruch, M.J., Koprak, S.L., Fischer, P.A., and Sigal, N.H. (1990a). The immunosuppressive macrolides FK-506 and rapamycin act as reciprocal antagonists in murine T cells. J. Immunol. 144, 1418-1424.
34. Dumont, F.J., Staruch, M.J., Koprak, S.L., Melino, M.R., and Sigal, N.H. (1990b). Distinct mechanisms of suppression of murine T cell activation by the related macrolides FK-506 and rapamycin. J. Immunol. 144, 251-258.
35. Dumont, F.J., Staruch, M.J., Koprak, S.L., Siekierka, J.J., Lin, C.S., Harrison, R., Sewell, T., Kindt, V.M., Beattie, T.R., Wyvratt, M., et al. (1992). The immunosuppressive and toxic effects of FK-506 are mechanistically related: pharmacology of a novel antagonist of FK-506 and rapamycin. J. Exp. Med. 176, 751-760.
36. Ferris, C.D., Huganir, R.L., Bredt, D.S., Cameron, A.M., and Snyder, S.H. (1991). Inositol triphosphate receptor: phosphorylation by protein kinase C and calcium calmodulin-dependent protein kinases in reconstituted lipid vesicles. Proc. Natl. Acad. Sci. USA 88, 2232-2235.
37. Ferris, C.D., Cameron, A.M., Bredt, D.S., Huganir, R.L., and Snyder, S.H. (1992). Autophosphorylation of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 267, 7036-7041.
38. Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., and Schmid, F.X. (1989). Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337, 476-478.
39. Freeman, B.C., Toft, D.O., and Morimoto, R.I. (1996). Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274, 1718-1720.
40. Friedman, J., and Weissman, I. (1991). Two cytoplasmic candidates for immunophilin action are revealed by affinity for a new cyclophilin: one in the presence and one in the absence of CsA. Cell 66, 799-806.
41. Fung, J.J., and Starzl, T.E. (1994). FK 506 in solid organ transplantation. Transplant. Proc. 26, 3017-3020.
42. Galat, A., Lane, W.S., Standaert, R.F., and Schreiber, S.L. (1992). A rapamycin-selective 25-kDa immunophilin. Biochemistry 31, 2427-2434.
43. Gerlach, M., Riederer, P., Pzuntek, H., and Youdim, M.B. (1991). MPTP mechanisms of neurotoxicity and their implications for Parkinson's disease. Eur. J. Pharmacol. 208, 273-286.
44. Gold, B.G., Storm-Dickerson, T., and Austin, D.R. (1994). The immunosuppressant FK506 increases functional recovery and nerve regeneration following peripheral nerve injury. Restor. Neurol. Neurosci. 6, 287-296.
45. Gold, B.G., Katoh, K., and Storm-Dickerson, T. (1995). The immunosuppressant FK506 increases the rate of axonal regeneration in rat sciatic nerve. J. Neurosci. 15, 7509-7516.
46. Gold, B.G., Zeleny-Pooley, M., Wang, M.-S., Chaturvedi, P., and Armistead, D.M. (1997). A nonimmunosuppressant FKBP-12 ligand increases nerve regeneration. Exp. Neurol. 147, 269-278.
47. Goldner, F.M., and Patrick, J.W. (1996). Neuronal localization of the cyclophilin A protein in the adult rat brain. J. Comp. Neurol. 372, 283-293.
48. Handschumacher, R.E., Harding, M.W., Rice, J., Drugge, R.J., and Speicher, D.W. (1984). Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226, 544-547.
49. Harding, M.W., Galat, A., Uehling, D.E., and Schreiber, S.L. (1989). A receptor for the immunosuppressant FK506 is acis-trans peptidylprolyl isomerase. Nature 341, 758-760.
50. Hartley, K.O., Gell, D., Smith, G.C., Zhang, H., Divecha, N., Connelly, M.A., Admon, A., Lees-Miller, S.P., Anderson, C.W., and Jackson, S.P. (1995). DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82, 849-856.
51. Heitman, J., Movva, N.R., and Hall, M.N. (1991). Targets for cell cyclearrest by the immunosuppressant rapamycin in yeast. Science 253, 905-909.
52. Henrich-Noack, P., Prehn, J.H., and Krieglstein, J. (1996). TGF-beta 1 protects hippocampal neurons against degeneration caused by transient global ischemia. Dose-response relationship and potential neural protective mechanisms. Stroke 27, 1609-1614.
53. Hirsch, D.B., Steiner, J.P., Dawson, T.M., Mammen, A., Hayek, E., and Snyder, S.H. (1993). Neurotransmitter release regulated by nitric oxide in PC12 cells and brain synaptosomes. Curr. Biol. 3, 749-754.
54. Jayaraman, T., Brillantes, A.M., Timerman, A.P., Fleischer, S., Erdjument-Bromage, H., Tempst, P., and Marks, A.R. (1992). FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 267, 9474-9477.
55. Jefferies, H.B., Reinhard, C., Kozma, S.C., and Thomas, G. (1994). Rapamycin selectively represses translation of the "polypyrimidine tract" mRNA family. Proc. Natl. Acad. Sci. USA 91, 4441-4445.
56. Jin, Y.J., and Burakoff, S.J. (1993). The 25-kDa FK506-binding protein is localized in the nucleus and associates with casein kinase II and nucleolin. Proc. Natl. Acad. Sci. USA 90, 7769-7773.
57. Jin, Y.J., Albers, M.W., Lane, W.S., Bierer, B.E., Schreiber, S.L., and Burakoff, S.J. (1991). Molecular cloning of a membrane-associated human FK506-and rapamycin-binding protein, FKBP-13. Proc. Natl. Acad. Sci. USA 88, 6677-6681.
58. Kay, J.E. (1996). Structure-function relationships in the FK506-binding protein (FKBP) family of peptidylprolyl cis-trans isomerases. Biochem. J. 314, 361-385.
59. Kay, J.E., Benzie, C.R., and Borghetti, A.F. (1983). Effect of cyclosporine A on lymphocyte activation by the calcium ionophore A23187. Immunology 50, 441-446.
60. Klauck, T.M., Faux, M.C., Labudda, K., Langeberg, L.K., Jaken, S., and Scott, J.D. (1996). Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 271, 1589-1592.
61. Kunz, J., Henriquez, R., Schneider, U., Deuter-Reinhard, M., Movva, N.R., and Hall, M.N. (1993). Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 73, 585-596.
62. Kuo, C.J., Chung, J., Fiorentino, D.F., Flanagan, W.M., Blenis, J., and Crabtree, G.R. (1992). Rapamycin selectively inhibits interleukin-2 activation of p70 S6 kinase. Nature 358, 70-73.
63. Lai, M.M., Burnett, P.E., Wolosker, H., Blackshaw, S., and Snyder, S.H. (1998). Cain, a novel physiologic protein inhibitor of calcineurin. J. Biol. Chem. 273, 18325-18331.
64. Lam, E., Martin, M.M., Timerman, A.P., Sabers, C., Fleischer, S., Lukas, T., Abraham, R.T., O'Keefe, S.J., O'Neill, E.A., and Wiederrecht, G.J. (1995). A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J. Biol. Chem. 270, 26511-26522.
65. Lavin, M.F., Khanna, K.K., Beamish, H., Spring, K., Watters, D., and Shiloh, Y. (1995). Relationship of the ataxia-telangiectasia protein ATM to phosphoinositide 3 kinase. Trends Biochem. Sci. 20, 382-383.
66. Liu, J., Farmer, J.D., Jr., Lane, W.S., Friedman, J., Weissman, I., and Schreiber, S.L. (1991). Calcineurin is acommon target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 807-815.
67. Liu, J.P., Sim, A.T., and Robinson, P.J. (1994). Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science 265, 970-973.
68. Lyons, W.E., George, E.B., Dawson, T.M., Steiner, J.P., and Snyder, S.H. (1994). Immunosuppressant FK506 promotes neurite outgrowth in cultures of PC12 cells and sensory ganglia. Proc. Natl. Acad. Sci. USA 91, 3191-3195.
69. Lyons, W.E., Steiner, J.P., Snyder, S.H., and Dawson, T.M. (1995). Neuronal regeneration enhances the expression of the immunophilin FKBP-12. J. Neurosci. 15, 2985-2994.
70. Massagué, J. (1996). TGFβ signaling: receptors, transducers, and Mad proteins. Cell 85, 947-950.
71. Morris, P.J. (1991). Cyclosporine, FK-506 and other drugs in organ transplantation. Curr. Opin. Immunol. 3, 748-751.
72. Nakanishi, H., Obaishi, H., Satoh, A., Wada, M., Mandai, K., Satoh, K., Nishioka, H., Matsuura, Y., Mizoguchi, A., and Takai, Y. (1997). Neurabin: a novel neural tissue-specific actin filament-binding protein involved in neurite formation. J. Cell Biol. 139, 951-961.
73. Nichols, R.A., Suplick, G.R., and Brown, J.M. (1994). Calcineurin-mediated protein dephosphorylation in brain nerve terminals regulates the release of glutamate. J. Biol. Chem. 269, 23817-23823.
74. Okadome, T., Oeda, E., Saitoh, M., Ichijo, H., Moses, H.L., Miyazono, K., and Kawabata, M. (1996). Characterization of the interaction of FKBP12 with the transforming growth factor-beta type I receptor in vivo. J. Biol. Chem. 271, 21687-21690.
75. Prehn, J.H., Bindokas, V.P., Jordan, J., Galindo, M.F., Ghadge, G.D., Roos, R.P., Boise, L.H., Thompson, C.B., Krajewski, S., Reed, J.C., et al. (1996). Protective effects of transforming growth factor-beta 1 on beta-amyloid neurotoxicity in rat hippocampal neurons. Mol. Pharmacol. 49, 319-328.
76. Price, E.R., Zydowsky, L.D., Jin, M.J., Baker, C.H., McKeon, F.D., and Walsh, C.T. (1991). Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence. Proc. Natl. Acad. Sci. USA 88, 1903-1907.
77. Ren, R.F., and Flanders, K.C. (1996). Transforming growth factors-beta protect primary rat hippocampal neuronal cultures from degeneration induced by beta-amyloid peptide. Brain Res. 732, 16-24.
78. Robinson, P.J., Sontag, J.-M., Liu, J.-P., Fykse, E.M., Slaughter, C., McMahon, H., and Sudhof, T.C. (1993). Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Science 365, 163-166.
79. Sabatini, D.M., Erdjument-Bromage, H., Lui, M., Tempst, P., and Sndyer, S.H. (1994). RAFT1 : a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 78, 35-43.
80. Sabatini, D.M., Pierchala, B.A., Barrow, R.K., Schell, M.J., and Snyder, S.H. (1995). The rapamycin and FKBP12 target (RAFT) displays phosphatidylinositol 4-kinase activity. J. Biol. Chem. 270, 20875-20878.
81. Sabatini, D.M., Blackshaw, S., Barrow, R.K., Fields, M., Kirsh, J., Betz, H., and Snyder, S.H. (1996). RAFT-1 interactions with the clustering protein gephyrin are required for rapamycin-sensitive signaling. In NEN Symposium on Signal Transduction (Boston: NEN Du-Pont), pp. 5-6.
82. Sabers, C.J., Martin, M.M., Brunn, G.J., Williams, J.M., Dumont, F.J., Wiederrecht, G., and Abraham, R.T. (1995). Isolation of a protein target of the FKBP12-rapamycin complex in mammalian cells. J. Biol. Chem. 270, 815-822.
83. Schreiber, S.L. (1991). Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science 251, 283-287.
84. Sharkey, J., and Butcher, S.P. (1994). Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature 371, 336-339.
85. Shou, W., Aghdasi, B., Armstrong, D.L., Guo, Q., Bao, S., Charng, M.-J., Mathews, L.M., Schneider, M.D., Hamilton, S.L., and Matzuk, M. (1998). Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 391, 489-492.
86. Siekierka, J.J., Hung, S.H., Poe, M., Lin, C.S., and Sigal, N.H. (1989a). A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin. Nature 341, 755-757.
87. Siekierka, J.J., Staruch, M.J., Hung, S.H., and Sigal, N.H. (1989b). FK-506, a potent novel immunosuppressive agent, binds to a cytosolic protein, which is distinct from the cyclosporin A-binding protein, cyclophilin. J. Immunol. 143, 1580-1583.
88. Smith, D.F., Albers, M.W., Schreiber, S.L., Leach, K.L., and Deibel, M.R., Jr. (1993). FKBP54, a novel FK506-binding protein in avian progesterone receptor complexes and HeLa extracts. J. Biol. Chem. 268, 24270-24273.
89. Snyder, S.H. (1977). Opiate receptors in the brain. New Eng. J. Med. 296, 266-271.
90. Snyder, S.H. (1992). Nitric oxide:first in a new class of neurotransmitters. Science 257, 494-496.
91. Sonenberg, N. (1996). mRNA 5′ CAP-binding protein EIF-4E and control of cell growth. In Translational Control, J.W.B. Hershey, M.B. Matthews, and N. Sonenberg, eds. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 245-269.
92. Stamnes, M.A., and Zuker, C.S. (1990). Peptidyl-prolyl cis-trans isomerases, cyclophilin, FK506-binding protein, and ninaA: four of a kind. Curr. Opin. Cell Biol. 2, 1104-1107.
93. Steiner, J.P., Dawson, T.M., Fotuhi, M., Glatt, C.E., Snowman, A.M., Cohen, N., and Snyder, S.H. (1992). High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature 358, 584-587.
94. Steiner, J.P., Dawson, T.M., Fotuhi, M., and Snyder, S.H. (1996). Immunophilin regulation of neurotransmitter release. Mol. Med. 2, 325-333.
95. Steiner, J.P., Connolly, M.A., Valentine, H.L., Hamilton, G.S., Dawson, T.M., Hester, L., and Snyder, S.H. (1997a). Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin A. Nature Med. 3, 421-428.
96. Steiner, J.P., Hamilton, G.S., Ross, D.T., Valentine, H.L., Guo, H., Connolly, M.A., Liang, S., Ramsey, C., Li, J.H., Huang, W., et al. (1997b). Neurotrophic immunophilin ligands stimulate structural and functional recovery in neurodegenerative animal models. Proc. Natl. Acad. Sci. USA 94, 2019-2024.
97. Tai, P.K., Albers, M.W., Chang, H., Faber, L.E., and Schreiber, S.L. (1992). Association of a 59-kilodalton immunophilin with the glucocorticoid receptor complex. Science 256, 1315-1318.
98. Takahashi, N., Hayano, T., and Suzuki, M. (1989). Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337, 473-475.
99. Terada, N., Patel, H.R., Takase, K., Kohno, K., Nairn, A.C., and Gelfand, E.W. (1994). Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc. Natl. Acad. Sci. USA 91, 11477-11481.
100. Thomson, A.W., and Starzl, T.E. (1992). FK 506 and autoimmune disease: perspective and prospects. Autoimmunity 12, 303-313.
101. Tocci, M.J., Matkovich, D.A., Collier, K.A., Kwok, P., Dumont, F., Lin, S., Degudicibus, S., Siekierka, J.J., Chin, J., and Hutchinson, N.I. (1989). The immunosuppressant FK506 selectively inhibits expression of early T cell activation genes. J. Immunol. 143, 718-726.
102. Urrutia, R., Henley, J.R., Cook, T., and McNiven, M.A. (1997). The dynamins: redundant or distinct functions for an expanding family of related GTPases? Proc. Natl. Acad. Sci. USA 94, 377-384.
103. von Manteuffel, S.R., Gingras, A.C., Ming, X.F., Sonenberg, N., and Thomas, G. (1996). 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 93, 4076-4080.
104. Wang, T., Donahoe, P.K., and Zervos, A.S. (1994). Specific interaction of type I receptors of the TGF-beta family with the immunophilin FKBP-12. Science 265, 674-676.
105. Wang, T., Li, B.Y., Danielson, P.D., Shah, P.C., Rockwell, S., Lechleider, R.J., Martin, J., Manganaro, T., and Donahoe, P.K. (1996). The immunophilin FKBP12 functions as a common inhibitor of the TGF beta family type I receptors. Cell 86, 435-444.
106. Yun, H.Y., Dawson, D.L., and Dawson, T.M. (1996). Neurobiology of nitric oxide. Crit. Rev. Neurobiol. 10, 291-316.
107. Zhang, F., Endo, S., Cleary, L.J., Eskin, A., and Byrne, J.H. (1997). Role of transforming growth factor-beta in long-term synaptic facilitation in Aplysia. Science 275, 1318-1320.