A novel immunophilin ligand: Distinct branching effects on dopaminergic neurons in culture and neurotrophic actions after oral administration in an animal model of Parkinson's disease

Neurobiology of Disease

Volumn 5, Issue 2, 1998, Pages 97-106

  Costantini, L C ^a   Chaturvedi, P ^b   Armistead, D M ^b   McCaffrey, P G ^b   Deacon, T W ^a   Isacson, O ^a  

^a MCLEAN HOSPITAL   (United States)

^b VERTEX PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; FK 506 BINDING PROTEIN; IMMUNOPHILIN; IMMUNOSUPPRESSIVE AGENT; LIGAND; TACROLIMUS;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN PROTECTION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; EMBRYO; EXPERIMENTAL MODEL; MOUSE; NERVE CELL CULTURE; NEUROLOGIC DISEASE; NONHUMAN; ORAL DRUG ADMINISTRATION; PARKINSON DISEASE; PRIORITY JOURNAL;

EID: 0031660913     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1006/nbdi.1998.0185     Document Type: Article

References (52)

1. Albers, K. M., Wright, D. E., & Davis, B. M. (1994) Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14, 1422-1432.
2. Altar, C. A., Boylan, C. B., Fritsche, M., Jones, B. E., Jackson, C., Weigand, S. J., Lindsay, R. M., & Hyman, C. (1994) Efficacy of brain-derived neurotrophic factor and neurotrophin-3 on neurochemical and behavioral deficits associated with partial nigrostriatal dopamine lesions. J. Neurochem. 63, 1021-1032.
3. Aoyagi, A., Nishikawa, K., Saito, H., & Abe, K. (1994) Characterization of basic fibroblast growth factor-mediated acceleration of axonal branching in cultures of rat hippocampal neurons. Brain Res. 661, 117-126.
4. Armistead, D. M., Badia, M. C., Deininger, D. D., Duffy, J. P., Saunders, J. O., Tung, R. D., Thomson, J. A., DeCenzo, M. T., Puter, O., Livingston, D. J., Murcko, M. A., Yamashita, M. M., & Navia, M. A. (1995) Design, synthesis, and structure of non-macrocyclic inhibitors of FKBP12, the major binding protein for the immunosuppressant FK506. Acta Crystallogr. D51, 522-528.
5. Backman, C., Rose, G. M., Hoffer, B. J., Henry, M. A., Bartus, R. T., Friden, P., & Granholm, A. C. (1996) Systemic administration of nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J. Neurosci. 16, 5437-5442.
6. Beck, K. D., Knusel, B., & Hefti, F. (1993) The nature of the trophic action of brain-derived neurotrophic factor, sed(1-3)-insulin-like growth factor-1, and basic fibroblast growth factor on mesencephalic dopaminergic neurons developing in culture. Neuroscience 52, 855-866.
7. Bixby, J. L., & Jhabvala, P. (1990) Extracellular matrix molecules and cell adhesion molecules induce neurites through different mechanisms. J. Cell Biol. 111, 2725-2732.
8. Brillantes, A. B., Ondrias, K., Scott, A., Kobrinsky, E., Ondriasova, E., Moschella, M. C., Jayaraman, T., Landers, M., Ehrlich, B. E., & Marks, A. R. (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513-523.
9. Cameron, A. M., Steiner, J. P., Sabatini, D. M., Kaplin, A. I., Walensky, L. D., & Snyder, S. H. (1995) Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Sci. USA 92, 1784-1788.
10. Date, I., Felton, D. L., & Felton, S. Y. (1990) Long-term effect of MPTP in the mouse brain in relation to aging: Neurochemical and immunocytochemical analysis. Brain Res. 519, 266-276.
11. Date, I., Yoshimoto, Y., Imaoko, T., Miyoshi, Y., Gohda, Y., Furuta, T., Asari, S., & Ohmoto, T. (1993) Enhanced recovery of the nigrostriatal dopaminergic system in MPTP-treated mice following intrastriatal injection of basic fibroblast growth factor in relation to aging. Brain Res. 621, 150-154.
12. Dawson, T. M., Steiner, J. P., Dawson, V. L., Dinerman, J. L., Uhl, G. R., & Snyder, S. H. (1993) Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate toxicity. Proc. Natl. Acad. Sci. USA 90, 9808-9812.
13. Frim, D. M., Uhler, T. A., Galpern, W. R., Beal, M. F., Breakefield, X. O., & Isacson, O. (1994) Implanted fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevent 1-methyl-4-phenylpyridinium toxicity to dopaminergic neurons in rat. Proc. Natl. Acad. Sci. USA 91, 5104-5108.
14. Galpern, W. R., Frim, D. M., Tatter, S. B., Altar, C. A., Beal, M. F., & Isacson, O. (1996) Cell-mediated delivery of brain-derived neurotrophic factor enhances dopamine levels in an MPP+ rat model of substantia nigra degeneration. Cell Transplant. 5, 225-232.
15. Gold, B. G., Katoh, K., & Storm-Dickerson, T. (1995) The immunosuppressant FK506 increases the rate of axonal regeneration in rat sciatic nerve. J. Neurosci. 15, 7509-7516.
16. Gold, B. G., Zeleny-Pooley, M., Wang, M. S., Chaturvedi, P., & Armistead, D. M. (1997) A non-immunosuppressive FKBP-12 ligand increases nerve regeneration. Exp. Neurol., 147, 269-278.
17. 11C]RTI-32 PET studies of the dopamine transporter in early dopa-naive Parkinson's disease: Implications for the symptomatic threshold. Neurology 48, 1578-1583.
18. Hemmendinger, L. M., Garber, B. B., Hoffmann, P. C., & Heller, A. (1981) Target neuron-specific process formation by embryonic mesencephalic dopamine neurons in vitro. Proc. Natl. Acad. Sci. USA 78, 1264-1268.
19. Hoffer, B. J., Hoffman, A., Bowenkamp, K., Huettl, P., Hudson, J., Martin, D., Lin, L. F., & Gerhardt, G. A. (1994) Glial cell-line derived neurotrophic factor reverses toxin-induced injury to midbrain dopaminergic neurons in vivo. Neurosci. Lett. 182, 107-111.
20. Hou, J. G., Lin, L. H., & Mytilineou, C. (1996) Glial cell-line derived neurotrophic factor exerts neurotrophic effects on dopaminergic neurons in vitro and promotes their survival and regrowth after damage by 1-methyl-4-phenylpyridinium. J. Neurochem. 66, 74-82.
21. Isaacson, L. G., Saffran, B. N., & Crutcher, K. A. (1992) Nerve growth factor-induced sprouting of mature uninjured sympathetic axons. J. Comp. Neurol. 326, 327-336.
22. Jamil, G., Hagar, R., Kaftan, E. J., & Ehrlich, B. E. (1996) Effects of FK506 analogs on ryanodine receptors. Biophys. J. 70, A75.
23. Jayaraman, T., Brillantes, A., Timerman, A. P., Fleischer, S., Erdjument-Bromage, H., Tempst, P., Marks, A. R. (1992) FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol Chem. 267, 9474-9477.
24. Johnson, E. M., Koike, T., & Franklin, J. (1992) The "calcium set-point hypothesis" of neuronal dependence on neurotrophic factor. Exp. Neurol. 115, 163-166.
25. Kearns, C. M., & Gash, D. M. (1995) GDNF protects nigral dopamine neurons against 6-hydroxydopamine in vivo. Brain Res. 672, 104-111.
26. Kitamura, Y., Itano, Y., Kubo, T., & Nomura, Y. (1994) Suppressive effect of FK506, a novel immunosuppressant, against MPTP-induced dopamine depletion in the striatum of young C57BL6 mice. J. Neuroimmunol. 50, 221-224.
27. Kreiglstein, K., Suter-Crazzolara, C., Fischer, W. H., & Unsicker, K. (1995a) TGF-beta superfamily members promote survival of mid-brain dopaminergic neurons and protect them against MPP+ toxicity. The EMBO Journal 14, 736-742.
28. Kreiglstein, K., Suter-Crazzolara, C., Hotten, G., Pohl, J., & Unsicker, K. (1995b) Trophic and protective effects of growth/differentiation factor 5, a member of the transforming growth factor-beta superfamily, on midbrain dopaminergic neurons. J. Neurosci. Res. 42, 724-732.
29. Krieglstein, K., & Unsicker, K. (1994) Transforming growth factor-B promotes survival of midbrain dopaminergic neurons and protects them against N-methyl-4-phenylpiridinium ion toxicity. Neuroscience 63, 1189-1996.
30. Liu, J., M. W., A., Wandless, T. J., Alberg, D. G., Belshaw, P. J., Cohen, P., Mackintosh, C., Klee, C. B., & Schreiber, S. L. (1992) Inhibition of T cell signalling by immunophilin-ligand complexes correlates with loss of calcineurin phosphatase activity. Biochemistry 31, 3896-3901.
31. Lyons, W. E., George, E. B., Dawson, T. M., Steiner, J. P., & Snyder, S. H. (1994) Immunosuppressant FK506 promotes neurites outgrowth in cultures of PC12 cells and sensory ganglia. Proc. Natl. Acad. Sci. USA 91, 3191-3195.
32. Lyons, W. E., Steiner, J. P., Snyder, S. H., & Dawson, T. M. (1995) Neuronal regeneration enhances the expression of the immunophilin FKBP-12. J. Neurosci. 15, 2985-2994.
33. Marcaida, G., Kosenko, E., Minana, M. D., Grisolia, S., & Felipo, V. (1996) Glutamate induces calcienurin-mediated dephosphorylation of Na+, K(+)-ATPase that results in its activation in cerebellar neurons in culture. J. Neurochem. 66, 99-104.
34. Mattson, M. P. (1996) Calcium and free radicals: Mediators of neurotrophic factor and excitatory transmitter-regulated developmental plasticity and cell death. Perspect. Dev. Neurobiol. 3, 79-91.
35. Mattson, M. P., & Kater, S. B. (1987) Calcium regulation of neurite elongation and growth cone motility. J. Neurosci. 7, 4034-4043.
36. O'Keefe, S., Tamura, J., Kincaid, R. L., Tocci, M. J., & O'Neill, E. A. (1992) FK506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357, 692-694.
37. Otto, D., & Unsicker, K. (1993) FGF-2 modulates dopamine and dopamine-related striatal transmitter systems in the intact and MPTP-lesioned mouse. Eur. J. Neurosci. 5, 927-932.
38. Peattie, D. A., Harding, M. W., Fleming, M. A., DeCenzo, M. T., Lippke, J. A., Livingston, D. J., & Benasutti, M. (1992) Expression and characterization of human FKBP52, an immunophilin that associates with the 90-kDa heat shock protein and is a component of steroid receptor complexes. Proc. Natl Acad. Sci. USA 89, 10974-10978.
39. Rousselet, A., Felter, L., Chamak, B., & Prochiantz, A. (1988) Rat mesencephalic neurons in culture exhibit different morphological traits in the presence of media conditioned on mesencephalic or striatal astroglia. Dev. Biol 129, 495-504.
40. Sauer, H., Rosenblad, C., & Bjorklund, A. (1995) Glial cell-line derived neurotrophic factor but not transforming growth factor B3 prevents delayed degeneration of nigral dopaminergic neurons following striatal 6-hydroxydopamine lesion. Proc. Natl. Acad. Sci. USA 92, 8935-8939.
41. Seki, K., Chen, H. C., & Huang, K. P. (1995) Dephosphorylation of protein kinase C substrates, neurogranin, neuromodulin, and MARCKS, by calcineurin and protein phosphatases 1 and 2A. Arch. Biochem. Biophys. 316, 673-679.
42. Sharkey, J., & Butcher, S. P. (1994) Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature 371, 336-339.
43. Snyder, S. H., & Sabatini, D. M. (1995) Immunophilins and the nervous system. Nat. Med. 1, 32-37.
44. Steiner, J. P., Connelly, M. A., Valentine, H. L., Hamilton, G. S., Dawson, T. M., Hester, L., & Snyder, S. H. (1997a) Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin, and cyclosporin A. Nat. Med. 3, 421-428.
45. Steiner, J. P., Dawson, T. M., Fotuhi, M., Glatt, C. E., Snowman, A. M., Cohen, N., & Snyder, S. H. (1992) High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature 358, 584-586.
46. Steiner, J. P., Hamilton, G. S., Ross, D. T., Valentine, H. L., Guo, H., Connolly, M. A., Liang, S., Ramsey, C., Li, J. J., Huang, W., Howorth, P., Soni, R., Fuller, M., Sauer, H., Nowotnik, A. C., et al. (1997b) Neurotrophic immunophilin ligands stimulate structural and functional recovery in neurodegenerative animal models. Proc. Natl. Acad. Sci. USA 94, 2019-2024.
47. Studer, L., Spenger, C., Seiler, R. W., Altar, C. A., Lindsay, R. M., & Hyman, C. (1995) Comparison of the effects of the neurotrophins on the morphological structure of dopaminergic neurons in cultures of rat substantia nigra. Eur. J. Neurosci. 7, 223-233.
48. Tatton, W. G., & Greenwood, C. E. (1991) Rescue of dying neurons: A new action for deprenyl in MPTP parkinsonism. J. Neurosci. Res. 30, 666-672.
49. Tomac, A., Lindquist, E., Lin, L. F., Ogren, S. O., Young, D., Hoffer, B. J., & Olson, L. (1995) Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373, 33-339.
50. Wang, M. S., Zeleny-Pooley, M., & Gold, B. G. (1997) Comparative dose-dependence study of FK506 and cyclosporin A on the rate of axonal regeneration in the rat sciatic nerve. J. Pharmacol. Exp. Ther. 282, 1084-1093.
51. Wang, T., Li, B., Danielson, P. D., Shah, P. C., Rockwell, S., Lechleider, R. J., Martin, J., Manganaro, T., & Donahoe, P. K. (1996) The immunophilin FKBP12 functions as a common inhibitor of the TGF-beta family type I receptors. Cell 86, 435-444.
52. Yu, C., & Crutcher, K. A. (1995) Nerve growth factor immunoreactivity and sympathetic sprouting in the rat hippocampal formation. Brain Res. 672, 55-67.