Serotonin regulates the secretion and autocrine action of a neuropeptide to activate MAPK required for long-term facilitation in Aplysia

Neuron

Volumn 43, Issue 3, 2004, Pages 373-385

  Hu, Jiang Yuan ^a   Glickman, Leonard ^a   Wu, Fang ^a   Schacher, Samuel ^a  

^a New York State Psychiat I ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ANISOMYCIN; AUTORECEPTOR; CHELERYTHRINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; K 252A; KT 5720; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NEUROPEPTIDE; PROTEIN KINASE C INHIBITOR; PROTEIN SYNTHESIS INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; RAPAMYCIN; SEROTONIN; TYROSINE KINASE RECEPTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; APLYSIA; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FACILITATION; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN SYNTHESIS; SENSORY NERVE CELL; VARICOSIS;

AMINO ACID SEQUENCE; ANIMALS; APLYSIA; AUTOCRINE COMMUNICATION; CELLS, CULTURED; ENZYME ACTIVATION; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; NEURONS, AFFERENT; NEUROPEPTIDES; SEROTONIN; SYNAPSES;

EID: 4043060050     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2004.07.011     Document Type: Article

References (84)

1. Angers S., Fioravante D., Chin J., Cleary L.J., Bean A.J., Byrne J.H. Serotonin stimulates phosphorylation of Aplysia synapsin and alters its subcellular distribution. J. Neurosci. 22:2002;5412-5422
2. Bacskai B.J., Hochner B., Mahaut-Smith M., Adams S.R., Kaang B.K., Kandel E.R., Tsien R.Y. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science. 260:1993;222-226
3. Bailey C.H., Kaang B.K., Chen M., Martin K.C., Lim C.S., Casadio A., Kandel E.R. Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron. 18:1997;913-924
4. Balkowiec A., Katz D.M. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci. 22:2002;10399-10407
5. Barbas D., DesGroseillers L., Castellucci V.F., Carew T.J., Marinesco S. Multiple serotonergic mechanisms contributing to sensitization in Aplysia. evidence of diverse serotonin receptor subtypes Learn. Mem. 10:2003;373-386
6. Bartsch D., Casadio A., Karl K.A., Serodio P., Kandel E.R. CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell. 95:1998;211-223
7. Bedi S.S., Salim A., Chen S., Glanzman D.L. Long-term effects of axotomy on excitability and growth of isolated Aplysia sensory neurons in cell culture. potential role of cAMP J. Neurophysiol. 79:1998;1371-1383
8. Bergold P.J., Beushausen S.A., Sacktor T.C., Cheley S., Bayley H., Schwartz J.H. A regulatory subunit of the cAMP-dependent protein kinase down-regulated in Aplysia sensory neurons during long-term sensitization. Neuron. 8:1992;387-397
9. Bernier L., Castellucci V.F., Kandel E.R., Schwartz J.H. Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′:5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia. J. Neurosci. 2:1982;1682-1691
10. Braha O., Dale N., Hochner B., Klein M., Abrams T.W., Kandel E.R. Second messengers involved in the two processes of presynaptic facilitation that contribute to sensitization and dishabituation in Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA. 87:1990;2040-2044
11. Brunet J.F., Shapiro E., Foster S.A., Kandel E.R., Iino Y. Identification of a peptide specific for Aplysia sensory neurons by PCR-based differential screening. Science. 252:1991;856-859
12. Casadio A., Martin K.C., Giustetto M., Zhu H., Chen M., Bartsch D., Bailey C.H., Kandel E.R. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell. 99:1999;221-237
13. Cedar H., Schwartz J.H. Cyclic adenosine monophosphate in the nervous system of Aplysia californica. II. Effect of serotonin and dopamine. J. Gen. Physiol. 60:1972;570-587
14. Chain D.G., Schwartz J.H., Hegde A.N. Ubiquitin-mediated proteolysis in learning and memory. Mol. Neurobiol. 20:1999;125-142
15. Chang D.J., Li X.C., Lee Y.S., Kim H.K., Kim U.S., Cho N.J., Lo X., Weiss K.R., Kandel E.R., Kaang B.K. Activation of a heterologously expressed octopamine receptor coupled only to adenylyl cyclase produces all the features of presynaptic facilitation in Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA. 97:2000;1829-1834
16. Chin J., Angers A., Cleary L.J., Eskin A., Byrne J.H. TGF-beta1 in Aplysia. role in long-term changes in the excitability of sensory neurons and distribution of TbetaR-II-like immunoreactivity Learn. Mem. 6:1999;317-330
17. Chin J., Angers A., Cleary L.J., Eskin A., Byrne J.H. Transforming growth factor beta1 alters synapsin distribution and modulates synaptic depression in Aplysia. J. Neurosci. 22:2002;RC220
18. Dale N., Schacher S., Kandel E.R. Long-term facilitation in Aplysia involves increase in transmitter release. Science. 239:1988;282-285
19. Dash P.K., Hochner B., Kandel E.R. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature. 345:1990;718-721
20. Davis S., Vanhoutte P., Pages C., Caboche J., Laroche S. The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J. Neurosci. 20:2000;4563-4572
21. Du J., Feng L., Yang F., Lu B. Activity- and calcium-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons. J. Cell Biol. 150:2000;1423-1434
22. Dyer J.R., Manseau F., Castellucci V.F., Sossin W.S. Serotonin persistently activates the extracellular signal-related kinase in sensory neurons of Aplysia independently of cAMP or protein kinase C. J. Neurosci. 116:2003;13-17
23. Emptage N.J., Carew T.J. Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science. 262:1993;253-256
24. English J.D., Sweatt J.D. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J. Biol. Chem. 272:1997;19103-19106
25. Evans G.J., Morgan A. Regulation of the exocytotic machinery by cAMP-dependent protein kinase. implications for presynaptic plasticity Biochem. Soc. Trans. 31:2003;824-827
26. Frey U., Huang Y.Y., Kandel E.R. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science. 260:1993;1661-1664
27. Gartner A., Staiger V. Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns. Proc. Natl. Acad. Sci. USA. 99:2002;6386-6391
28. Glanzman D.L., Kandel E.R., Schacher S. Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron. 3:1989;441-450
29. Glanzman D.L., Kandel E.R., Schacher S. Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science. 249:1990;799-802
30. Goldsmith B.A., Abrams T.W. Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylyl cyclase. Proc. Natl. Acad. Sci. USA. 88:1991;9021-9025
31. Goodman L.J., Valverde J., Lim F., Geschwind M.D., Federoff H.J., Geller A.I., Hefti F. Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons. Mol. Cell. Neurosci. 7:1996;222-238
32. Greenberg S.M., Castellucci V.F., Bayley H., Schwartz J.H. A molecular mechanism for long-term sensitization in Aplysia. Nature. 329:1987;62-65
33. Han W., Ng Y.K., Axelrod D., Levitan E.S. Neuropeptide release by efficient recruitment of diffusing cytoplasmic secretory vesicles. Proc. Natl. Acad. Sci. USA. 96:1999;14577-14582
34. Hegde A.N., Inokuchi K., Pei W., Casadio A., Ghirardi M., Chain D.G., Martin K.C., Kandel E.R., Schwartz J.H. Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell. 89:1997;115-126
35. Hu J.Y., Meng X., Schacher S. Target interaction regulates distribution and stability of specific mRNAs. J. Neurosci. 22:2002;2669-2678
36. Huang Y.Y., Martin K.C., Kandel E.R. Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J. Neurosci. 20:2000;6317-6325
37. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron. 21:1998;869-883
38. Jovanovic J.N., Czernik A.J., Fienberg A.A., Greengard P., Sihra T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci. 3:2000;323-329
39. Kandel E.R., Schwartz J.H. Molecular biology of learning. modulation of transmitter release Science. 218:1982;433-443
40. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662
41. Kang H., Welcher A.A., Shelton D., Schuman E.M. Neurotrophins and time. different roles for TrkB signaling in hippocampal long-term potentiation Neuron. 19:1997;653-664
42. Khan A., Pepio A.M., Sossin W.S. Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysia synaptosomes. J. Neurosci. 21:2001;382-391
43. Kim J.H., Udo H., Li H.L., Youn T.Y., Chen M., Kandel E.R., Bailey C.H. Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron. 40:2003;151-165
44. Kohara K., Kitamura A., Morishima M., Tsumoto T. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science. 291:2001;2419-2423
45. Lee S.H., Han J.H., Choi J.H., Huh E.Y., Kwon Y.K., Kaang B.K. The effect of brain-derived neurotrophic factor on neuritogenesis and synaptic plasticity in Aplysia neurons and the hippocampal cell line HiB5. Mol. Cells. 15:2003;233-239
46. Lessmann V., Gottmann K., Malcangio M. Neurotrophin secretion. current facts and future prospects Prog. Neurobiol. 69:2003;341-374
47. Lin H., Bao J., Ying J.S., Walters E.T., Ambron R.T. Rapid electrical and delayed molecular signals regulate the serum response element after nerve injury. convergence of injury and learning signals J. Neurobiol. 57:2003;204-220
48. Liu J., Schwartz J.H. The cytoplasmic polyadenylation element binding protein and polyadenylation of mRNA in Aplysia neurons. Brain Res. 959:2003;68-76
49. Liu K., Hu J.Y., Wang D., Schacher S. Protein synthesis at synapse versus cell body. enhanced but transient expression of long-term facilitation at isolated synapses J. Neurobiol. 56:2003;275-286
50. Liu J., Hu J.Y., Schacher S., Schwartz J.H. The two regulatory subunits of Aplysia protein kinase A mediate distinct functions in producing synaptic plasticity. J. Neurosci. 24:2004;2465-2474
51. Martin K.C., Michael D., Rose J.C., Barad M., Casadio A., Zhu H., Kandel E.R. MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron. 18:1997;899-912
52. Meyer-Franke A., Wilkinson G.A., Kruttgen A., Hu M., Munro E., Hanson M.G. Jr., Reichardt L.F., Barres B.A. Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron. 21:1998;681-693
53. Michael D., Martin K.C., Seger R., Ning M.M., Baston R., Kandel E.R. Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia. Proc. Natl. Acad. Sci. USA. 95:1998;1864-1869
54. Minichiello L., Calella A.M., Medina D.L., Bonhoeffer T., Klein R., Korte M. Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron. 36:2002;121-137
55. Moccia R., Chen D., Lyles V., Kapuya E., Kalachikov S., Spahn C.M., Frank J., Kandel E.R., Barad M., Martin K.C. An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J. Neurosci. 23:2003;9409-9417
56. Montarolo P.G., Goelet P., Castellucci V.F., Morgan J., Kandel E.R., Schacher S. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science. 234:1986;1249-1254
57. Morozov A., Muzzio I.A., Bourtchouladze R., Van-Strien N., Lapidus K., Yin D., Winder D.G., Adams J.P., Sweatt J.D., Kandel E.R. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron. 39:2003;309-325
58. Muller U., Carew T.J. Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron. 21:1998;1423-1434
59. Murray B., Alessandrini A., Cole A.J., Yee A.G., Furshpan E.J. Inhibition of the p44/42 MAP kinase pathway protects hippocampal neurons in a cell-culture model of seizure activity. Proc. Natl. Acad. Sci. USA. 95:1998;11975-11980
60. Nazif F.A., Byrne J.H., Cleary L.J. cAMP induces long-term morphological changes in sensory neurons of Aplysia. Brain Res. 539:1991;324-327
61. Patterson S.L., Pittenger C., Morozov A., Martin K.C., Scanlin H., Drake C., Kandel E.R. Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron. 32:2001;123-140
62. Purcell A.L., Sharma S.K., Bagnall M.W., Sutton M.A., Carew T.J. Activation of a tyrosine kinase-MAPK cascade enhances the induction of long-term synaptic facilitation and long-term memory in Aplysia. Neuron. 37:2003;473-484
63. Roberson E.D., English J.D., Adams J.P., Selcher J.C., Kondratick C., Sweatt J.D. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci. 19:1999;4337-4348
64. Rosenblum K., Futter M., Voss K., Erent M., Skehel P.A., French P., Obosi L., Jones M.W., Bliss T.V. The role of extracellular regulated kinases I/II in late-phase long-term potentiation. J. Neurosci. 22:2002;5432-5441
65. Santarelli L., Montarolo P., Schacher S. Neuropeptide localization in varicosities of Aplysia sensory neurons is regulated by target and neuromodulators evoking long-term synaptic plasticity. J. Neurobiol. 31:1996;297-308
66. Schacher S., Kandel E.R., Montarolo P. cAMP and arachidonic acid simulate long-term structural and functional changes produced by neurotransmitters in Aplysia sensory neurons. Neuron. 10:1993;1079-1088
67. Schacher S., Wu F., Panyko J.D., Sun Z.Y., Wang D. Expression and branch-specific export of mRNA are regulated by synapse formation and interaction with specific postsynaptic targets. J. Neurosci. 19:1999;6338-6347
68. + channels of Aplysia sensory neurons in cell-free membrane patches. Nature. 313:1985;392-395
69. Si K., Giustetto M., Etkin A., Hsu R., Janisiewicz A.M., Miniaci M.C., Kim J.H., Zhu H., Kandel E.R. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia. Cell. 115:2003;894-904
70. Sometani A., Kataoka H., Nitta A., Fukumitsu H., Nomoto H., Furukawa S. Transforming growth factor-beta1 enhances expression of brain-derived neurotrophic factor and its receptor, TrkB, in neurons cultured from rat cerebral cortex. J. Neurosci. Res. 66:2001;369-376
71. 2+- activated PKCs in Aplysia neurons by 5-HT. J. Neurosci. 12:1992;1160-1168
72. Steffensen I., Syed N.I., Lukowiak K., Bulloch A.G., Morris C.E. Sensorin-A immunocytochemistry reveals putative mechanosensory neurons in Lymnaea CNS. Invert. Neurosci. 1:1995;207-213
73. Sugita S., Goldsmith J.R., Baxter D.A., Byrne J.H. Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation in sensorimotor connections of Aplysia. J. Neurophysiol. 68:1992;643-651
74. Sun Z.Y., Wu F., Schacher S. Rapid bidirectional modulation of mRNA expression and export accompany long-term facilitation and depression of Aplysia synapses. J. Neurobiol. 46:2001;41-47
75. Sutton M.A., Carew T.J. Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory neuron synapses in Aplysia. Neuron. 26:2000;219-231
76. Sweatt J.D., Kandel E.R. Persistent and transcriptionally-dependent increase in protein phosphorylation in long-term facilitation of Aplysia sensory neurons. Nature. 339:1989;51-54
77. Tapley P., Lamballe F., Barbacid M. K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene. 7:1992;371-381
78. Waltereit R., Weller M. Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol. Neurobiol. 27:2003;99-106
79. Walters E.T., Bodnarova M., Billy A.J., Dulin M.F., Diaz-Rios M., Miller M.W., Moroz L.L. Somatotopic organization and functional properties of mechanosensory neurons expression sensorin-A mRNA in Aplysia californica. J. Comp. Neurol. 471:2004;219-240
80. Yamamoto N., Hegde A.N., Chain D.G., Schwartz J.H. Activation and degradation of the transcription factor C/EBP during long-term facilitation in Aplysia. J. Neurochem. 73:1999;2415-2423
81. Yanow S.K., Manseau F., Hislop J., Castellucci V.F., Sossin W.S. Biochemical pathways by which serotonin regulates translation in the nervous system of Aplysia. J. Neurochem. 70:1998;572-583
82. Zakharenko S.S., Patterson S.L., Dragatsis I., Zeitlin S.O., Siegelbaum S.A., Kandel E.R., Morozov A. Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron. 39:2003;975-990
83. Zhang F., Endo S., Cleary L.J., Eskin A., Byrne J.H. Role of transforming growth factor-beta in long-term synaptic facilitation in Aplysia. Science. 275:1997;1318-1320
84. Zhu H., Wu F., Schacher S. Expression and distribution of Aplysia cell adhesion molecules can influence synapse formation and elimination in vitro. J. Neurosci. 15:1995;4173-4183