Immunophilin ligands and GDNF enhance neurite branching or elongation from developing dopamine neurons in culture

Experimental Neurology

Volumn 164, Issue 1, 2000, Pages 60-70

  Costantini, L C ^a,b   Isacson, O ^a,b  

^a MCLEAN HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Calcineurin; Dopamine cultures; FK506; FKBP12; GDNF; Immunophilin; Neurite; Rapamycin

Indexed keywords

CALCINEURIN; CYCLOSPORIN A; DOPAMINE; FK 506 BINDING PROTEIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; IMMUNOPHILIN; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; RAPAMYCIN; TACROLIMUS;

ANIMAL CELL; ARTICLE; CELL INTERACTION; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG EFFECT; GROWTH STIMULATION; IMMUNOCYTOCHEMISTRY; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FIBER REGENERATION; NERVE SPROUTING; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT;

EID: 0033942955     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.2000.7417     Document Type: Article

References (80)

1. Aoyagi A., Nishikawa K., Saito H., Abe K. Characterization of basic fibroblast growth factor-mediated acceleration of axonal branching in cultured rat hippocampal neurons. Brain Res. 661:1994;117-126
2. Apostilides C., Sanford E., Hong M., Mendez I. Glial cell line-derived neurotrophic factor improves intrastriatal graft survival of stored dopaminergic cells. Neuroscience. 83:1998;363-372
3. Armistead D. M., Badia M. C., Deininger D. D., Duffy J. P., Saunders J. O., Tung R. D., Thomson J. A., DeCenzo M. T., Futer O., Livingston D. J., Murcko M. A., Yamashita M. M., Navia M. A. Design, synthesis, and structure of non-macrocyclic inhibitors of FKBP12, the major binding protein for the immunosuppressant FK506. Acta. Crystallogr. D51:1995;522-528
4. Baloh R., Tansey M., Golden J., Creedon D., Heuckeroth R., Keck C., Zimonjic D., Popescu N., Johnson E., Milbrandt H. TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret. Neuron. 18:1997;793-802
5. Beck K. D., Knusel B., Hefti F. 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. 52:1993;855-866
6. Benowitz L. I., Routtenberg A. GAP-43: An intrinsic determinant of neuronal development and plasticity. Trends NeuroScience 20:1997;84-91
7. Brillantes A. B., Ondrias K., Scott A., Kobrinsky E., Ondriasova E., Moschella M. C., Jayaraman T., Landers M., Ehrlich B. E., Marks A. R. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell. 77:1994;513-523
8. Cameron A. M., Steiner J. P., Sabatini D. M., Kaplin A. I., Walensky L. D., Snyder S. H. Immunophilin FK506 binding protein associated with inositol 1, 4, 5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Science USA. 92:1995;1784-1788
9. Chang H., Takei K., Sydor A., Born T., Rusnak F., Jay D. Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature. 376:1995;686-690
10. Costantini L., Chaturvedi P., Armistead D., McCaffrey P., Deacon T., Isacson O. 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. Neurobiol. Dis. 5:1998;97-106
11. Costantini L. C., Lin L., Isacson O. Medial fetal ventral mesencephalon: A preferred source for dopamine neuron grafts. Neuroreport. 8:1997;2253-2257
12. 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 toxicity. Proc. Natl. Acad. Science USA. 90:1993;9808-9812
13. Dawson T. M., Steiner J. P., Lyons W. E., Fotuhi M., Blue M., Snyder S. H. The immunophilins, FK506 binding protein and cyclophilin, are discretely localized in the brain: Relationship to calcineurin. Neuroscience. 62:1994;569-580
14. Denis-Donini S., Glowinski J., Prochiantz A. Specific influence of striatal target neurons on the in vitro outgrowth of mesencephalic dopaminergic neurites: A morphological quantitative study. J. Neurochem. 3:1983;2292-2299
15. Dumont F., Melino M., Staruch M., Koprak S., Fischer P., Sigal N. The immunosuppressive macrolides FK506 and rapamycin act as reciprocal antagonists in murine T cells. J. Immunol. 144:1990;1418-1424
16. Ebendal T., Tomac A., Hoffer B., Olson L. Glial cell line-derived neurotrophic factor stimulates fiber formation and survival in cultured neurons from peripheral autonomic ganglia. J. NeuroScience Res. 40:1995;276-284
17. Engele J. Spatial and temporal growth factor influences on developing midbrain dopaminergic neurons. J. NeuroScience Res. 53:1998;405-414
18. Feng L., Wang C., Jiang H., Oho C., Mizuno K., Dugich-Djordjevic M., Lu B. Differential effects of GDNF and BDNF on cultures ventral mesencephalic neurons. Mol. Brain Res. 66:1999;62-70
19. Ferreira A., Kincaid R., Kosik K. Calcineurin is associated with the cytoskeleton of cultured neurons and has a role in the acquisition of polarity. Mol. Biol. Cell. 4:1993;1225-1238
20. Fruman D., Klee C., Bierer B., Burakoff S. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK506 and cyclosporin A. Proc. Natl. Acad. Science 89:1992;3686-3690
21. Funauchi M., Haruta H., Tsumoto T. Effects of an inhibitor for calcium/calmodulin-dependent protein phosphatase, calcineurin, on induction of long-term potentiation in rat visual cortex. NeuroScience Res. 19:1994;269-278
22. Galat A., Lane W., Standaert R., Schreiber S. A rapamycin-selective 25-kDa immunophilin. Biochemistry. 31:1992;2427-2434
23. Gallo G., Letourneau P. Axon guidance: GTPases help axons reach their targets. Curr. Biol. 8:1998;R80-R82
24. Gold B., Densmore V., Shou W., Matzuk M., Gordon H. Immunophilin FK506-binding protein 52 (not FK506-binding protein 12) mediates the neurotrophic action of FK506. J. Pharmacol. Exp. Ther. 289:1999;1202-1210
25. Gold B. G., Katoh K., Storm-Dickerson T. The immunosuppressant FK506 increases the rate of axonal regeneration in rat sciatic nerve. J. NeuroScience 15:1995;7509-7516
26. Gold B. G., Zeleny-Pooley M., Wang M. S., Chaturvedi P., Armistead D. M. A non-immunosuppressive FKBP-12 ligand increases nerve regeneration. Exp. Neurol. 147:1997;269-278
27. Goto S., Matsukado Y., Mihara Y., Inoue N., Miyamoto E. The distribution of calcineurin in the rat brain by light and electron microscopic immunohistochemistry and enzyme-immunoassay. Brain Res. 397:1986;161-172
28. Goto S., Yammamoto H., Fukunaga K., Iwasa T., Matsukado Y., Miyamoto E. Dephosphorylation of microtubule-associated protein 2, tau factor, and tubulin by calcineurin. J. Neurochem. 45:1985;276-283
29. Granholm A., Mott J., Bowenkamp K., Eken S., Henry S., Hoffer B., Lapchak P., Palmer M., van Horne C., Gerhardt G. Glial cell line-derived neurotrophic factor improves survival of ventral mesencephalic grafts to the 6-hydroxydopamine lesioned striatum. Exp. Brain Res. 116:1997;29-38
30. Halpain S., Hipolito A., Saffer L. Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J. NeuroScience 18:1998;9835-9844
31. Handschumacher R., Harding M., Rice J., Drugge R., Speicher D. Cyclophilin: A specific cytosolic binding protein for cyclosporin A. Science. 1984;544-547
32. 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. 341:1989;758-760
33. Helekar S. A., Char D., Neff S., Patrick J. Prolyl isomerase requirement for the expression of functional homo-oligomeric ligand-gated ion channels. Neuron. 12:1994;179-189
34. Hemmendinger L. M., Garber B. B., Hoffmann P. C., Heller A. Target neuron-specific process formation by embryonic mesencephalic dopamine neurons in vitro. Proc. Natl. Acad. Science USA. 78:1981;1264-1268
35. Hiwasa T., Kondo K., Hishiki T., Koshizawa S., Umezawa K., Nakagawara A. GDNF-induced neurite formation was stimulated by protein kinase inhibitors and suppressed by Ras inhibitors. NeuroScience Lett. 238:1997;115-118
36. Hou J. G., Lin L. H., Mytilineou C. 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. 66:1996;74-82
37. Jamil G., Hagar R., Kaftan E. J., Ehrlich B. E. Effects of FK506 analogs on ryanodine receptors. Biophys. J. 70:1996;A75
38. Jayaraman T., Brillantes A., Timerman A. P., Fleischer S., Erdjument-Bromage H., Tempst P., Marks A. R. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 267:1992;9474-9477
39. Jing S., Wen D., Yu Y., Holst P., Luo Y., Fang M., Tamir R., Antonia L., Hu Z., Cupples R., Louis J., Hu S., Altrock B., Fox G. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell. 85:1996;1113-1124
40. Johansson M., Friedemann M., Hoffer B., Stromberg I. Effects of glial cell line-derived neurotrophic factor on developing and mature ventral mesencephalic grafts in oculo. Exp. Neurol. 134:1995;25-34
41. Johnson E. M., Koike T., Franklin J. The "calcium set-point hypothesis" of neuronal dependence on neurotrophic factor. Exp. Neurol. 115:1992;163-166
42. King M., Huang C., Chock P., Nairn A., Hemmings H., Chan K., Greengard P. Mammalian brain phosphoproteins as substrates for calcineurin. J. Biol. Chem. 10:1984;8080-8083
43. Kreiglstein K., Suter-Crazzolara C., Fischer W. H., Unsicker K. TGF-beta superfamily members promote survival of midbrain dopaminergic neurons and protect them against MPP+ toxicity. EMBO J. 14:1995;736-742
44. Leclere P., Ekstrom P., Edstrom A., Priestly J., Averill S., Tonge D. Effects of glial cell line-derived neurotrophic factor on axonal growth and apoptosis in adult mammalian sensory neurons in vitro. Neuroscience. 82:1997;545-558
45. Letourneau P. The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect. Dev. Neurobiol. 4:1996;111-123
46. Lin L., Doherty D., Lile J., Bektesh S., Collins F. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science. 260:1993;1130-1132
47. Lin L., Zhang T., Collins F., Armes L. Purification and initial characterization of rat B49 glial cell line-derived neurotrophic factor. J. Neurochem. 63:1994;758-768
48. Liu J., Farmer J., Lane W., Friedman J., Weissman I., Schreiber S. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell. 66:1991;807-815
49. Lo D. Instructive roles of neurotrophins in synaptic plasticity. Prog. Brain Res. 117:1998;65-70
50. Lyons W. E., George E. B., Dawson T. M., Steiner J. P., Snyder S. H. Immunosuppressant FK506 promotes neurites outgrowth in cultures of PC12 cells and sensory ganglia. Proc. Natl. Acad. Science USA. 91:1994;3191-3195
51. Maness P., Beggs H., Klinz S., Morse W. Selective neural cell adhesion molecule signalling by Src family tyrosine kinases and tyrosine phosphatases. Perspect. Dev. Neurobiol. 4:1996;169-181
52. Marcaida G., Kosenko E., Minana M. D., Grisolia S., Felipo V. Glutamate induces calcineurin-mediated dephosphorylation of Na+, K(+)-ATPase that results in its activation in cerebellar neurons in culture. J. Neurochem. 66:1996;99-104
53. Mattson M. P. Calcium as sculptor and destroyer of neural circuitry. Exp. Gerontol. 27:1992;29-49
54. Mattson M. P., Guthrie P. B., Kater S. B. Components of neurite outgrowth that determine neuronal cytoarchitecture: Influence of calcium and the growth substrate. J. NeuroScience Res. 20:1988;331-345
55. Mattson M. P., Kater S. B. Calcium regulation of neurite elongation and growth cone motility. J. NeuroScience 7:1987;4034-4043
56. Meberg P., Ono S., Minamide L., Takahashi M., Bamburg J. Actin depolymerization factor and cofilin phosphorylation dynamics: Response to signals that regulate neurite extension. Cell Motil. Cytoskeleton. 39:1998;172-190
57. Newman-Gage H., Graybiel A. Expression of calcium/calmodulin-dependent protein kinase in relation to dopamine islands and synaptic maturation in the cat striatum. J. NeuroScience 8:1988;3360-3375
58. Nichols R., Suplick G., Brown J. Calcineurin-mediated protein dephosphorylation in brain nerve terminals regulates release of glutamate. J. Biol. Chem. 269:1994;23, 817-23, 823
59. O'Leary D., Koester S. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron. 10:1993;991-1006
60. Rehder V., Kater S. Regulation of neuronal growth cone filopodia by intracellular calcium. J. NeuroScience 12:1992;1375-1386
61. Rosenblad C., Martinez-Serrano A., Bjorklund A. Glial cell line-derived neurotrophic factor increases survival, growth and function of intrastriatal fetal nigral dopaminergic grafts. Neuroscience. 75:1996;979-985
62. Rousselet A., Felter L., Chamak B., Prochiantz A. Rat mesencephalic neurons in culture exhibit different morphological traits in the presence of media conditioned on mesencephalic or striatal astroglia. Dev. Biol. 129:1988;495-504
63. Sautter J., Tseng J., Braguglia D., Aebischer P., Spenger C., Seiler R., Widmer H., Zurn A. Implants of polymer-encapsulated genetically modified cells releasing glial cell line-derived neurotrophic factor improve survival, growth, and function of fetal dopaminergic grafts. Exp. Neurol. 149:1998;230-236
64. Seki K., Chen H. C., Huang K. P. Dephosphorylation of protein kinase C substrates, neurogranin, neuromodulin, and MARCKS, by calcineurin and protein phosphatases 1 and 2A. Arch. Biochem. Biophys. 316:1995;673-679
65. Sharkey J., Butcher S. P. Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature. 371:1994;336-339
66. Sharp A., Nucifora F., Blondel O., Sheppard C., Zhang C., Snyder S., Russell J., Ryugo D., Ross C. Differential cellular expression of isoforms of inositol 1, 4, 5-triphosphate receptors in neurons and glia in brain. J. Comp. Neurol. 406:1999;207-220
67. Steiner J. P., Connelly M. A., Valentine H. L., Hamilton G. S., Dawson T. M., Hester L., Snyder S. H. Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin, and cyclosporin A. Nat. Med. 3:1997;421-428
68. Steiner J. P., Dawson T. M., Fotuhi M., Glatt C. E., Snowman A. M., Cohen N., Snyder S. H. High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature. 358:1992;584-586
69. Steiner J. P., Dawson T. M., Fotuhi M., Snyder S. H. Immunophilin regulation of neurotransmitter release. Mol. Science 2:1996;325-333
70. 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., Suzdak P. D. Neurotrophic immunophilin ligands stimulate structural and functional recovery in neurodegenerative animal models. Proc. Natl. Acad. Science USA. 94:1997;2019-2024
71. Studer L., Spenger C., Seiler R. W., Altar C. A., Lindsay R. M., Hyman C. Comparison of the effects of the neurotrophins on the morphological structure of dopaminergic neurons in cultures of rat substantia nigra. Eur. J. NeuroScience 7:1995;223-233
72. Tai P., Albers M., Chang H., Faber L., Schreiber S. Association of a 59-kDa immunophilin with the glucocorticoid receptor complex. Science. 256:1992;1315-1318
73. Torii N., Kamashita T., Otsu Y., Tsumoto T. An inhibitor of calcineurin, FK506, blocks induction of long-term depression in rat visual cortex. Neuroscience. 185:1995;1-4
74. Treanor J., Goodman L., deSauvage F., Stone D., Poulson K., Bexk C., Gray C., Armanini M., Pollock R., Hefti F., Phillips H., Goddard A., Moore M., Buj-Bello A., Davies A., Asai N., Takahashi M., Vandlen R., Henderson C., Rosenthal A. Characterization of a multicomponent receptor for GDNF. Nature. 382:1996;80-83
75. van Weering D., Bos J. Glial cell line-derived neurotrophic factor induces Ret-mediated lamellipodia formation. J. Biol. Chem. 272:1997;249-254
76. Voorn P., Kalsbeek A., Jorritsma-Byham B., Groenewegen H. The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience. 25:1988;857-887
77. Walensky L., Gascard P., Fields M., Blackshaw S., Conboy J., Mohandas N., Snyder S. The 13-kD FK506 binding protein, FKBP13, interacts with a novel homologue of the erythrocyte membrane cytoskeletal protein 4.1. J. Cell Biol. 141:1998;143-153
78. 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 the rat sciatic nerve. J. Pharmacol. Exp. Ther. 282:1997;1084-1093
79. Widenfalk J., Nosrat C., Tomac A., Westphal H., Hoffer B., Olson L. Neurturin and glial cell line-derived neurotrophic factor receptor beta, novel proteins related to GDNF and GDNFR-alpha with specific cellular patterns of expression suggesting roles in the developing and adult nervous system and in peripheral organs. J. NeuroScience 17:1997;8506-8519
80. Wilby M., Sinclaie S., Muir E., Zietlow R., Adcock K., Horellou P., Rogers J., Dunnett S., Fawcett J. A glial cell line-derived neurotrophic factor-secreting clone of the Schwann cell line SCTM41 enhances survival and fiber outgrowth from embryonic nigral neurons grafted to the striatum and to the lesioned substantia nigra. J. NeuroScience 19:1999;2301-2312