FK506 AND THE ROLE OF THE IMMUNOPHILIN FKBP-52 IN NERVE REGENERATION*

REFERENCES

• Gold B. G. FK506 and the role of immunophilins in nerve regeneration. Mol. Neurobiol. 1997; 15: 285–306
   PubMed Web of Science ®Google Scholar
• Kino T., Hatanaka H., Nishiyama H. FK-506, a novel immunosuppressant isolated from a streptomyces. I. Fermentation, isolation, and physio-chemical and biological characteristics. J. Antibiot. 1987; 40: 1249–1255
   PubMed Web of Science ®Google Scholar
• Kino T., Hatanaka H., Miyata S., Inamura N., Nishiyama M., Yajima T., Goto T., Okuhara M., Kohsaka M., Aoki H., Ochiai T. FK-506, a novel immunosuppressant isolated from a streptomyces. II. Immunosuppressive effect of FK-506. in vitro J. Antibiot. 1987; 40: 1256–1265
   PubMed Web of Science ®Google Scholar
• Hoffman A. L., Makowka L., Banner B., Cai X., Cramer D. V., Pascualone A., Todo S., Starzl T. E. The use of FK-506 for small intestine allotransplantation: Inhibition of acute rejection and prevention of fatal graft-versus-host disease. Transplantation 1990; 49: 483–490
   PubMed Web of Science ®Google Scholar
• Starzl T. E., Makowka L., Todo S. A potential breakthrough in immunosuppression. Transplant. Proc. 1987; 19: S3–S104
   Web of Science ®Google Scholar
• Starzl T. E., Todo S., Fung J., Demetris A. J., Venkataramman R., Jain A. FK-506 for liver, kidney, and pancreas transplantation. Lancet 1989; 2: 1000–1004
   PubMed Web of Science ®Google Scholar
• Kino T., Goto T. Discovery of FK-506 and update. Ann. NY Acad. Sci. 1993; 685: 13–21
   PubMed Web of Science ®Google Scholar
• McDiarmid S. V., Busutti R. W., Ascher N. L., Burdick A. J., D'Alessandro A. M., Esquivel C., Kalayoglu M., Klein A. S., Marsh J. W., Miller C. M., Schwartz M. E., Shaw B. W., So S. K. FK506 (tacrolimus) compared with cyclosporine for primary immunosuppression after pediatric liver transplantation. Transplantation 1995; 59: 530–536
   PubMed Web of Science ®Google Scholar
• Shapiro R., Fung J. J., Jain A. B., Parks P., Todo S., Starzl T. E. The side effects of FK506 in humans. Transplant. Proc. 1990; 22: 35–36
   PubMed Web of Science ®Google Scholar
• Schreiber S. L., Crabtree G. R. The mechanism of action of cyclosporin A and FK506. Immunol. Today 1992; 13: 136–142
   PubMedGoogle Scholar
• Schreiber S. L. Chemistry and Biology of the immunophilins and their immunosuppressive ligands. Science 1991; 251: 283–287
   PubMed Web of Science ®Google Scholar
• Alnemri E. S., Fernandes-Alnemri T., Nelki D. S., Dudley K., DuBois G. C., Litwack G. Overexpression, characterization, and purification of a recombinant mouse immunophilin FKBP-52 and identification of an associated phosphoprotein. Proc. Natl. Acad. Sci. USA 1993; 90: 6839–6843
   PubMed Web of Science ®Google Scholar
• Sigal N. H., Dumont F. J., Cyclosporin A. FK-506, and Rapamycin: Pharmacologic probes of lymphocyte signal transduction. Annu. Rev. Imnunol. 1992; 10: 519–560
   PubMed Web of Science ®Google Scholar
• Freman D. A., Klee C. B., Bierer B. E., Burakoff S. J. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK506 and cyclosporin A. Proc. Natl. Acad. Sci. USA 1992; 89: 3686–3690
   PubMed Web of Science ®Google Scholar
• Dyck P. J., Lais A. C., Karnes J. L., Sparks M., Hunter H., Low P. A. Permanent axotomy, a model of axonal atrophy and secondary segmental demyelination and remyelination. Ann. Neurol. 1981; 19: 575–583
   Google Scholar
• Liu J., Farmer J. D., Lane W. S., Friedman J., Weissman I., Schreiber S. L. Calcineurin is a comnon target of cyclophilin–cyclosporin A and FKBP–FK506 complexes. Cell 1991; 66: 807–815
   PubMed Web of Science ®Google Scholar
• Walsh C. T., Zydowsky L. D., McKeon F. D. Cyclosporin A, the cyclophilin class of peptidylprolyl isomerases, and blockade of T cell signal transduction. J. Biol. Chem. 1992; 267: 13,115–13,118
   Google Scholar
• Terada N., Or R., Weinberg K., Domenico J., Lucas J. J., Gelfand E. W. Transcription of IL-4 genes is not inhibited by cyclosporin A in competent T cells. J. Biol. Chem. 1992; 267: 21,207–21,210
   Google Scholar
• Tocci M. J., Matkovich D. A., Matkovich K., Collier K. A., Kwok P., Dumont F., Lin S., Degudicibus S., Siekerka J. J., Chin J., Hutchinson N. I. The immunosuppressant FK506 selectively inhibits expression of early T cell activation genes. J. Immunol. 1989; 143: 718–726
   PubMed Web of Science ®Google Scholar
• Steiner J. P., Dawson T. M., Fotuhi M., Glatt C. M., Snowman A. M.M., Cohen N., Snyder S. H. High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature 1992; 358: 584–587
   PubMed Web of Science ®Google Scholar
• Lyons W. E., Steiner J. P., Snyder S. H., Dawson T. M. Neuronal regeneration enhances the expression of the imnunophilin FKBP-12. J. Neurosci. 1995; 15: 2985–2994
   PubMed Web of Science ®Google Scholar
• Sánchez E. R., Ning Y.-M. Immunophilins, heat shock protein, and glucocorticoid receptor actions in vivo. Methods Enzymol 1996; 9: 188–200
   Google Scholar
• Snyder S. H., Sabatini D. M. Immunophilins and the nervous system. Nature Med. 1995; 1: 32–37
   PubMed Web of Science ®Google Scholar
• Wiederrecht G., Etzkorn F. The immunophilins. Perspect. Drug Discov. Des. 1994; 2: 57–84
   Google Scholar
• Harding M. W., Galat A., Uehling D. E., Schreiber S. L. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 1989; 341: 758–760
   PubMed Web of Science ®Google Scholar
• Siekierka J. J., Hung S. H.Y., Poe M., Lin C. S., Sigal N. H. A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolylisomerase activity but is distinct from cyclophilin. Nature 1989; 341: 755–757
   PubMed Web of Science ®Google Scholar
• Siekierka J. J., Wiederrecht G., Greulich H., Boulton D., Hung S. H.Y., Cryan J., Hodges P. J., Sigal N. H. The cytosolic-binding protein for the immunosuppressant FK-506 is both a ubiquitous and highly conserved peptidyl-prolyl cis-trans isomerase. J. Biol. Chem 1990; 265: 21,011–21,015
   Google Scholar
• Lyons W. E., Steiner J. P., Dawson T. M., Snyder S. H. Increased expression of FK-506 binding protein during peripheral nerve regeneration. Soc. Neurosci. Abstr 1992; 18: 604
   Google Scholar
• Klee C. B. Concerted regulation of protein phosphorylation and dephosphorylation by calmodulin. Neurochem. Res 1991; 16: 1059–1065
   PubMed Web of Science ®Google Scholar
• Gold B. G., Storm-Dickerson T., Austin D. R., Katoh K. FK506, an immunosuppressant, increases functional recovery and axonal regeneration in the rat following axotomy of the sciatic nerve. Soc. Neurosci. Abstr 1993; 19: 1316
   Google Scholar
• Gold B. G., Storm-Dickerson T., Austin D. R. The immunosuppressant FK506 increases functional recovery and nerve regeneration following peripheral nerve injury. Restor. Neurol. Neurosci 1994; 6: 287–296
   PubMed Web of Science ®Google Scholar
• Gold B. G., Katoh K., Storm-Dickerson T. The immunosuppressant FK506 increases the rate of axonal regeneration in rat sciatic nerve. J. Neurosci 1995; 15: 7505–7509
   Google Scholar
• Wang M. S., Zeleny-Pooley M., Gold B. G. Comparative dose-dependence study of FK506 and cyclosporin A on the rate of axonal regeneration in rat sciatic nerve. J. Pharmacol. Exp. Ther. 1997; 282: 1084–1093
   PubMed Web of Science ®Google Scholar
• Carreau A., Gueugnon J., Benavides J., Vigé X. Comparative effects of FK-506, rapamycin and cyclosporin A, on the in vitro differentiation of dorsal root ganglia explants and septal cholinergic neurons. Neuropharmacology 1997; 36: 1755–1762
   PubMed Web of Science ®Google Scholar
• Steiner J. P., Connolly M. A., Valentine H. L., Hamilton G. S., Dawson T. M., Hester L., Snyder S. H. Neurotrophic actions of nonimmunosuppressive ligands of immunophilins. Nature Med 1997; 3: 1–8
   PubMedGoogle Scholar
• Steiner J. P., Hamilton G. S., Ross D. T., Valentine H. L., Guo H., Connolly M. A., Liang S., Ramsey C., Li J., Huang W., Howorth P., Soni R., Fuller M., Sauer H., Nowotnik A. C., Suzdak P. D. Neurotrophic immunophilin ligands stimulate structural and functional recovery in neurodegenerative animal models. Proc. Natl. Acad. Sci. USA 1997; 94: 2019–2024
   PubMed Web of Science ®Google Scholar
• Gold B. G., Zeleny-Pooley M., Wang M.-S., Chaturvedi P., Armistead D. M. A nonimmunosuppressant FKBP-12 ligand increases nerve regeneration. Exp. Neurol 1997; 147: 269–278
   PubMed Web of Science ®Google Scholar
• Cameron A. M., Nucifora F. C., Jr., Fung E. T., Livingston D. J., Aldape R. A., Ross C. A., Snyder S. H. FKBP12 binds the inositol 1,4,5-trisphosphate receptor at leucine-proline(1400–1401) and anchors calcineurin to this FK506-like domain. J. Biol. Chem 1997; 272: 27,582–27,588
   Google Scholar
• Shou W., Agihdasi B., Armstron D. L., Guo Q., Bao S., Charng M.-J., Mathews L. M., Schneider M. D., Hamilton S. L., Matsuk M. M. Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 1998; 391: 489–492
   PubMed Web of Science ®Google Scholar
• Gold B. G., Densmore V., Shou W., Matzuk M. M., Gordon H. S. Immunophilin FK506 binding protein 52 (not FK506 binding protein 12) mediates the neurotrophic action of FK506. J. Pharmacol. Exp. Therap 1999; 289: 1202–1210
   PubMed Web of Science ®Google Scholar
• Jones K. J. Gonadal steroids as promoting factors in axonal regeneration. Brain Res. Bull 1993; 30: 491–498
   PubMed Web of Science ®Google Scholar
• Pratt W. B., Toft D. O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev 1997; 18: 306–360
   PubMed Web of Science ®Google Scholar
• Pratt W. B. The hsp90-based chaperone system: Involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med 1998; 217: 420–434
   PubMed Web of Science ®Google Scholar
• Scheibel T., Weikl T., Buchner J. Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc. Natl. Acad. Sci. USA 1998; 95: 1495–1499
   PubMed Web of Science ®Google Scholar
• Raaka B. M., Finnerty M., Sun E., Samuels H. H. Effects of molybdate on steroid receptors in intact GH1 cells. J. Biol. Chem 1985; 260: 14,009–14,015
   Google Scholar
• Gold B. G., Yew J. Y., Zeleny-Pooley M. The immunosuppressant FK506 increases GAP-43 mRNA levels in axotomized sensory neurons. Neuroscience 1998; 241: 25–28
   Web of Science ®Google Scholar
• Benowitz L. I., Routtenberg A. GAP-43: An intrinsic determinant of neuronal development and plasticity. Trends Neurosci 1997; 20: 84–91
   PubMed Web of Science ®Google Scholar
• Yao G. L., Kiyama H. Dexamethasone enhances level of GAP-43 mRNA after nerve injury and facilitates re-projection of the hypoglossal nerve. Mol. Brain Res 1995; 32: 308–312
   PubMedGoogle Scholar
• Jones K. J., Drengler S. M., Oblinger M. M. Gonadal steroid regulation of growth-associated protein GAP-43 mRNA expression in axotomized hamster facial motor neurons. Neurochem. Res 1997; 22: 1367–1374
   PubMed Web of Science ®Google Scholar
• Eggen B. J. L., Nielander H. B., Rensen-de Leeuw M. G. A., Chotman S. P., Gispen W. H., Schrama L. H. Identification of two promoter regions in the rat B-50/GAP-43 gene. Mol. Brain Res 1994; 23: 221–234
   PubMedGoogle Scholar
• Herdegen T., Skene P., Böhr M. The c-jun transcription factor—bipotential mediator of neuronal death, survival and regeneration. Trends Neurosci. 1997; 20: 227–231
   PubMed Web of Science ®Google Scholar
• Yardin C., Terro F., Lesort M., Esclaire F., Hugon J. FK506 antagonizes apoptosis and c-jun protein expression in neuronal cultures. NeuroReport 1998; 9: 2077–2080
   PubMed Web of Science ®Google Scholar
• Dawson T. M., Steiner J. P., Dawson V. L., Dinerman J. L., Uhl G. R., Snyder S. H. Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc. Natl. Acad. Sci. USA 1993; 90: 9808–9812
   PubMed Web of Science ®Google Scholar
• Sharkey J., Butcher S. P. Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature 1994; 371: 336–339
   PubMed Web of Science ®Google Scholar
• Ide T., Morikawa E., Kirino T. An immunosuppressant, FK506, protects hippocampal neurons from forebrain ischemia in the Mongolian gerbil. Neurosci. Lett 1996; 204: 157–160
   PubMed Web of Science ®Google Scholar
• Tokime T., Nozaki K., Kikuchi H. Neuroprotective effect of FK506, an immunosuppressant, on transient global ischemia in gerbil. Neurosci. Lett 1996; 206: 81–84
   PubMed Web of Science ®Google Scholar
• Yagita Y., Kitagawa K., Matsushita K., Taguchi A., Mabuchi T., Ohtsuki T., Yanagihara T., Matsumoto M. Effect of immunosuppressant FK506 on ischemia-induced degeneration of hippocampal neurons in gerbils. Life Sci 1996; 59: 1643–1650
   PubMed Web of Science ®Google Scholar
• Sharkey J., Crawford J. H., Butcher S. P., Marston H. M. Tacrolimus (FK506) ameliorates skilled motor deficits produced by middle cerebral artery occlusion in rats. Stroke 1996; 27: 2282–2286
   PubMed Web of Science ®Google Scholar
• Kuroda S., Siesjo B. K. Postischemic administration of FK506 reduces infarct volume following transient focal brain ischemia. Neurosci. Res. Commun 1996; 19: 83–90
   Google Scholar
• Butcher S. P., Henshall D. C., Teramura Y., Iwasaki K., Sharkey J. Neuroprotective actions of FK506 in experimental stroke: In vivo evidence against an antiexcitotoxic mechanism. J. Neurosci. 1997; 17: 6939–6946
   PubMed Web of Science ®Google Scholar
• Obermann W. M. J., Sondermann H., Russo A. A., Pavletich N. P., Hartl F. U. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J. Cell Biol 1998; 143: 901–910
   PubMed Web of Science ®Google Scholar
• Tai P.-K. K., Chang H., Albers M. W., Schreiber S. L., Toft D. O., Faber L. E. P59 (FK506 binding protein 59) interaction with heat shock proteins is highly conserved and may involve proteins other than steroid receptors. Biochemistry 1993; 32: 8842–8847
   PubMed Web of Science ®Google Scholar
• Miyata Y., Chambraud B., Radanyi C., Leclerc J., Lebeau M.-C., Renoir J.-M., Shirai R., Catelli M.-G., Yahara I., Baulieu E.-E. Phosphorylation of the immunosuppressant FK506-binding protein FKBP52 by casein kinase II: Regulation of HSP90-binding activity of FKBP52. Proc. Natl. Acad. Sci. USA 1997; 94: 14,500–14,505
   Google Scholar
• Czar M. J., Owens-Grillo J. K., Yem A. W., Leach K. L., Deibel M. R., Jr., Welsh M. J., Pratt W. B. The hsp56 immunophilin component of untransformed steroid receptor complexes is localized both to microtubules in the cytoplasm and to the same nonrandom regions within the nucleus as the steroid receptor. Mol. Endocrin 1994; 8: 1731–1741
   PubMed Web of Science ®Google Scholar
• Dillman J. F., III, Dabney L. P., Pfister K. K. Cytoplasmic dynein is associated with slow axonal transport. Proc. Natl. Acad. Sci. USA 1996; 93: 141–144
   PubMed Web of Science ®Google Scholar
• Nixon R. A. The slow axonal transport of cytoskeletal proteins. Curr. Opin. Cell Biol. 1998; 10: 87–92
   PubMed Web of Science ®Google Scholar
• Sétáló G., Jr., Singh M., Warren M. F., Toran-Allerand D. Direct association of heat shock protein HSP90 and the extracellular signal regulated kinases, ERK1/2. A possible link between estrogen and neurotrophin signaling. Soc. Neurosci. Abstr 1997; 23: 1710
   Google Scholar
• Volonte C., Angelastro J. M., Greene L. A. Association of protein kinases ERK1 and ERK2 with p75 nerve growth factor receptors. J. Biol. Chem 1993; 268: 21,410–21,415
   Google Scholar
• Cowley S., Paterson H., Kemp P., Marshall C. J. Activation of MAP kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH3T3 cells. Cell 1994; 77: 841–852
   PubMed Web of Science ®Google Scholar
• York R. D., Yao H., Dillon T., Ellig C. L., Eckert S. P., McCleskey E. W., Stork P. J.S. Rapl mediates sustained MAP kinase activation induced by nerve growth factor. Nature 1998; 392: 622–626
   PubMed Web of Science ®Google Scholar
• Lyons W. E., George E. B., Dawson T. M., Steiner J. P., Snyder S. H. Immunosuppressant FK506 promotes neurite outgrowth in cultures of PC12 cells and sensory ganglia. Proc. Natl. Acad. Sci. USA 1994; 91: 3191–3195
   PubMed Web of Science ®Google Scholar
• Dittmar K. D., Demady D. R., Stancato L. F., Krishna P., Pratt W. B. Folding of the glucocorticoid receptor by the heat shock protein (hsp) 90-based chaperone machinery. J. Biol. Chem 1997; 272: 21,213–21,220
   Google Scholar
• Song Q., Alnemri E. S., Litwack G., Gilbert L. I. An immunophilin is a component of the insect ecdysone receptor (EcR) complex. Insect Biochem. Mol. Biol 1997; 27: 973–982
   PubMed Web of Science ®Google Scholar
• Kraft R., Levine R. B., Restifo L. L. The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J. Neurosci 1998; 18: 8886–8899
   PubMed Web of Science ®Google Scholar
• Vittorioso P., Cowling R., Faure J.-D., Caboche M., Bellini C. Mutation in the Arabidopsis PASTICCINO1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Mol. Cell Biol 1998; 18: 3034–3043
   PubMed Web of Science ®Google Scholar