Distinct roles of calcineurin-nuclear factor of activated T cells and protein kinase A - cAMP response element-binding protein signaling in presynaptic differentiation

Journal of Neuroscience

Volumn 25, Issue 12, 2005, Pages 3067-3079

  Yoshida, Tomoyuki ^a   Mishina, Masayoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Calcineurin; CREB; NFAT; Protein kinase A; Synapse formation; Zebrafish

Indexed keywords

CALCINEURIN; COMPLEMENTARY DNA; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOSPORIN A; ENHANCED GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MESSENGER RNA; NEUROMODULIN; SYNAPTOBREVIN; SYNAPTOBREVIN 2; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; NERVE ENDING; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SYNAPSE; TRANSGENIC ANIMAL; ZEBRA FISH;

AGE FACTORS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCINEURIN; CELL DIFFERENTIATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLOSPORINE; DIAGNOSTIC IMAGING; DNA-BINDING PROTEINS; EMBRYO; ENZYME INHIBITORS; GAP-43 PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MICROINJECTIONS; NFATC TRANSCRIPTION FACTORS; OLFACTORY RECEPTOR NEURONS; PRESYNAPTIC TERMINALS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 16244421669     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3738-04.2005     Document Type: Article

References (79)

1. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451.
2. Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C (1998) A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol Cell Biol 18:967-977.
3. Aramburu J, Yaffe MB, Lopez-Rodriguez C, Cantley LC, Hogan PG, Rao A (1999) Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285:2129-2133.
4. Bakalyar HA, Reed RR (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250:1403-1406.
5. Benfenati F, Valtorta F, Chieregatti E, Greengard P (1992) Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron 8:377-386.
6. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali E, Südhof TC (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531.
7. Billingsley ML, Kincaid RL (1997) Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem J 323:577-591.
8. Chang HY, Takei K, Sydor AM, Born T, Rusnak F, Jay DG (1995) Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature 376:686-690.
9. Clegg CH, Correll LA, Cadd GG, McKnight GS (1987) Inhibition of intracellular cAMP-dependent protein kinase using mutant genes of the regulatory type I subunit. J Biol Chem 262:13111-13119.
10. Clipstone NA, Crabtree GR (1992) Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357:695-697.
11. Dash PK, Hochner B, Kandel ER (1990) Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718-721.
12. Davis GW, Schuster CM, Goodman CS (1996) Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17:669-679.
13. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P (2003) Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6:708-716.
14. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K (1999) Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 19:8894-8908.
15. Dresbach T, Qualmann B, Kessels MM, Garner CC, Gundelfinger ED (2001) The presynaptic cytomatrix of brain synapses. Cell Mol Life Sci 58:94-116.
16. Dresbach T, Hempelmann A, Spilker C, tom Dieck S, Altrock WD, Zuschratter W, Garner CC, Gundelfinger ED (2003) Functional regions of the presynaptic cytomatrix protein bassoon: significance for synaptic targeting and cytomatrix anchoring. Mol Cell Neurosci 23:279-291.
17. Dynes JL, Ngai J (1998) Pathfinding of olfactory neuron axons to stereotyped glomerular targets revealed by dynamic imaging in living zebrafish embryos. Neuron 20:1081-1091.
18. Elferink LA, Scheller RH (1993) Synaptic vesicle proteins and regulated exocytosis. J Cell Sci Suppl 17:75-79.
19. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
20. Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737-752.
21. Garner CC, Kindler S, Gundelfinger ED (2000) Molecular determinants of presynaptic active zones. Curr Opin Neurobiol 10:321-327.
22. Graef IA, Chen F, Crabtree GR (2001) NFAT signaling in vertebrate development. Curr Opin Genet Dev 11:505-512.
23. Graef IA, Wang F, Charron F, Chen L, Neilson J, Tessier-Lavigne M, Crabtree GR (2003) Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 113:657-670.
24. Hall AC, Lucas FR, Salinas PC (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100:525-535.
25. Hammerschmidt M, Bitgood MJ, McMahon AP (1996) Protein kinase A is a common negative regulator of Hedgehog signaling in the vertebrate embryo. Genes Dev 10:647-658.
26. Hamori J, Somogyi J (1983) Differentiation of cerebellar mossy fiber synapses in the rat a quantitative electron microscope study. J Comp Neurol 220:365-377.
27. He Q, Dent EW, Meiri KF (1997) Modulation of actin filament behavior by GAP-43 (neuromodulin) is dependent on the phosphorylation status of serine 41, the protein kinase C site. J Neurosci 17:3515-3524.
28. Hiding H, Scheller RH (1996) Phosphorylation of synaptic vesicle proteins: modulation of the αSNAP interaction with the core complex. Proc Natl Acad Sci USA 93:11945-11949.
29. Hirokawa N, Sato-Yoshitake R, Kobayashi N, Pfister KK, Bloom GS, Brady ST (1991) Kinesin associates with anterogradely transported membranous organelles in vivo. J Cell Biol 114:295-302.
30. Ho AM, Jain J, Rao A, Hogan PG (1994) Expression of the transcription factor NFATp in a neuronal cell line and in the murine nervous system. J Biol Chem 269:28181-28186.
31. Hosaka M, Hammer RE, Südhof TC (1999) A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24:377-387.
32. Huang YY, Li XC, Kandel ER (1994) cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69-79.
33. Hummel T, Krukkert K, Roos J, Davis G, Klambt C (2000) Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26:357-370.
34. Jain J, McCaffrey PG, Miner Z, Kerppola TK, Lambert JN, Verdine GL, Curran T, Rao A (1993) The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365:352-355.
35. Jin Y (2002) Synaptogenesis: insights from worm and fly. Curr Opin Neurobiol 12:71-79.
36. Kawakami K, Noda T (2004) Transposition of the Tol2 element, an Ac-like element from the Japanese medaka fish Oryzias latipes, in mouse embryonic stem cells. Genetics 166:895-899.
37. Klee CB, Crouch TH, Krinks MH (1979) Calcineurin: a calcium- and calmodulin-binding protein of the nervous system. Proc Natl Acad Sci USA 76:6270-6273.
38. Kullberg RW, Lentz TL, Cohen MW (1977) Development of the myotomal neuromuscular junction in Xenopus laevis: an electrophysiological and fine-structural study. Dev Biol 60:101-129.
39. Kunz J, Hall MN (1993) Cyclosporin A, FK506 and rapamycin: more than just immunosuppression. Trends Biochem Sci 18:334-338.
40. Lautermilch NJ, Spitzer NC (2000) Regulation of calcineurin by growth cone calcium waves controls neurite extension. J Neurosci 20:315-325.
41. Liu J, Farmer JD, Lane WS, Friedman J, Weissman I, Schreiber SL (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807-815.
42. Liu YC, Storm DR (1989) Dephosphorylation of neuromodulin by calcineurin. J Biol Chem 264:12800-12804.
43. Lonart G, Schoch S, Kaeser PS, Larkin CJ, Südhof TC, Linden DJ (2003) Phosphorylation of RIM1α by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses. Cell 115:49-60.
44. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623.
45. Lyons WE, George EB, Dawson TM, Steiner JP, Snyder SH (1994) Immunosuppressant FK506 promotes neurite outgrowth in cultures of PC12 cells and sensory ganglia. Proc Natl Acad Sci USA 91:3191-3195.
46. Meiri KF, Pfenninger KH, Willard MB (1986) Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci USA 83:3537-3541.
47. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
48. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675-686.
49. 2+/ calmodulin-stimulable adenylyl cyclases as molecular coincidence detectors in memory formation. Cell Mol Life Sci 55:525-533.
50. Nakata T, Terada S, Hirokawa N (1998) Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J Cell Biol 140:659-674.
51. Namiki S, Tomida T, Tanabe M, lino M, Hirose K (2003) Intracellular delivery of glutathione S-transferase into mammalian cells. Biochem Biophys Res Commun 305:592-597.
52. Nishinakamura R, Matsumoto Y, Uochi T, Asashima M, Yokota T (1997) Xenopus FK 506-binding protein homolog induces a secondary axis in frog embryos, which is inhibited by coexisting BMP 4 signaling. Biochem Biophys Res Commun 239:585-591.
53. Nonet ML (1999) Visualization of synaptic specializations in live C. elegans with synaptic vesicle protein-GFP fusions. J Neurosci Methods 89:33-40.
54. Orellana SA, McKnight GS (1992) Mutations in the catalytic subunit of cAMP-dependent protein kinase result in unregulated biological activity. Proc Natl Acad Sci USA 89:4726-4730.
55. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493-497.
56. 2+-stimulated adenylyl cyclases in LTP and memory formation. Int J Dev Neurosci 19:387-394.
57. Ressler KJ, Sullivan SL, Buck LB (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245-1255.
58. Risinger C, Bennett MK (1999) Differential phosphorylation of syntaxin and synaptosome-associated protein of 25 kDa (SNAP-25) isoforms. J Neurochem 72:614-624.
59. Rodriguez I, Feinstein P, Mombaerts P (1999) Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199-208.
60. Roos J, Hummel T, Ng N, Klambt C, Davis GW (2000) Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26:371-382.
61. Sato-Yoshitake R, Yorifuji H, Inagaki M, Hirokawa N (1992) The phosphorylation of kinesin regulates its binding to synaptic vesicles. J Biol Chem 267:23930-23936.
62. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669.
63. Schiebler W, Jahn R, Doucet JP, Rothlein J, Greengard P (1986) Characterization of synapsin I binding to small synaptic vesicles. J Biol Chem 261:8383-8390.
64. Skene JH (1989) Axonal growth-associated proteins. Annu Rev Neurosci 12:127-156.
65. Song HJ, Poo MM (1999) Signal transduction underlying growth cone guidance by diffusible factors. Curr Opin Neurobiol 9:355-363.
66. Südhof TC, Czernik AJ, Kao HT, Takei K, Johnston PA, Horiuchi A, Kanazir SD, Wagner MA, Perin MS, De Camilli P, Greengard P (1989) Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245:1474-1480.
67. Takei Y, Harada A, Takeda S, Kobayash K, Terada S, Noda T, Takahashi T, Hirokawa N (1995) Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system. J Cell Biol 131:1789-1800.
68. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M (2002) Cadherin regulates dendritic spine morphogenesis. Neuron 35:77-89.
69. Tokuoka H, Yoshida T, Matsuda N, Mishina M (2002) Regulation by GSK-3β of the arborization field and maturation of retinotectal projection in zebrafish. J Neurosci 22:10324-10332.
70. tom Dieck S, Sanmarti-Vila L, Langnaese K, Richter K, Kindler S, Soyke A, Wex H, Smalla KH, Kampf U, Franzer JT, Stumm M, Garner CC, Gundelfinger ED (1998) Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J Cell Biol 142:499-509.
71. Ulloa L, Dombradi V, Diaz-Nido J, Szucs K, Gergely P, Friedrich P, Avila J (1993) Dephoshorylation of distinct sites on microtubule-associated protein MAP1B by protein phosphatases 1, 2A and 2B. FEBS Lett 330:85-89.
72. Umemori H, Linhoff MW, Ornitz DM, Sanes JR (2004) FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118:257-270.
73. Vardinon-Friedman H, Bresler T, Garner CC, Ziv NE (2000) Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69.
74. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall B, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991.
75. Wilson SW, Ross LS, Parrett T, Easter SSJ (1990) The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development 108:121-145.
76. Yan G, Chen X, Bancroft C (1994) A constitutively active form of CREB can activate expression of the rat prolactin promoter in non-pituitary cells. Mol Cell Endocrinol 101:R25-R30.
77. Yoshida T, Mishina M (2003) Neuron-specific gene manipulations in transparent zebrafish embryos. Methods Cell Sci 25:15-23.
78. Yoshida T, Ito A, Matsuda N, Mishina M (2002) Regulation by protein kinase A switching of axonal pathfinding of zebrafish olfactory sensory neurons through the olfactory placode-olfactory bulb boundary. J Neurosci 22:4964-4972.
79. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC (2001) Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29:131-143.