Signaling from synapse to nucleus: The logic behind the mechanisms

Current Opinion in Neurobiology

Volumn 13, Issue 3, 2003, Pages 354-365

  Deisseroth, Karl ^a   Mermelstein, Paul G ^b   Xia, Houhui ^a   Tsien, Richard W ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CASPASE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

APOPTOSIS; BIOCHEMISTRY; CELL DEATH; CELL MEMBRANE; CELL NUCLEUS; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CIRCADIAN RHYTHM; CONDITIONING; FEAR; GENE EXPRESSION; LEARNING; LONG TERM MEMORY; MEMORY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 0038391398     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(03)00076-X     Document Type: Review

References (84)

1. 2+-dependent regulation in neuronal gene expression. Curr Opin Neurobiol. 7:1997;419-429.
2. Bailey C.H., Bartsch D., Kandel E.R. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA. 93:1996;13445-13452.
3. West A.E., Griffith E.C., Greenberg M.E. Regulation of transcription factors by neuronal activity. Nat Rev Neurosci. 3:2002;921-931.
4. Bradley J., Finkbeiner S. An evaluation of specificity in activity-dependent gene expression in neurons. Prog Neurobiol. 67:2002;469-477.
5. Lonze B.E., Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron. 35:2002;605-623.
6. Morgan J.I., Curran T. Role of ion flux in the control of c-fos expression. Nature. 322:1986;552-555.
7. Crabtree G.R., Olson E.N. NFAT signaling: choreographing the social lives of cells. Cell. 109:2002;S67-S79.
8. Graef I.A., Mermelstein P.G., Stankunas K., Neilson J.R., Deisseroth K., Tsien R.W., Crabtree G.R. L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature. 401:1999;703-708.
9. 2+ channels in sympathetic neurons. Neuron. 1:1988;355-365.
10. 2+-regulated transcriptional repressor. Nature. 398:1999;80-84.
11. 2+-dependent nuclear signaling in neurons were obtained for translocation of the transcription factor itself [8] and translocation of an intermediate messenger [15].
12. •].
13. Wu G.Y., Deisseroth K., Tsien R.W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen- activated protein kinase pathway. Proc Natl Acad Sci USA. 98:2001;2808-2813.
14. Deisseroth K., Bito H., Tsien R.W. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron. 16:1996;89-101.
15. Deisseroth K., Heist E.K., Tsien R.W. Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature. 392:1998;198-202.
16. Ginty D.D., Kornhauser J.M., Thompson M.A., Bading H., Mayo K.E., Takahashi J.S., Greenberg M.E. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science. 260:1993;238-241.
17. Snutch T.P., Sutton K.G., Zamponi G.W. Voltage-dependent calcium channels - beyond dihydropyridine antagonists. Curr Opin Pharmacol. 1:2001;11-16.
18. Dolmetsch R.E., Pajvani U., Fife K., Spotts J.M., Greenberg M.E.
19. Hardingham G.E., Arnold F.J., Bading H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci. 4:2001;261-267.
20. Mermelstein P.G., Deisseroth K., Dasgupta N., Isaksen A.L., Tsien R.W. Calmodulin priming: nuclear translocation of a calmodulin complex and the memory of prior neuronal activity. Proc Natl Acad Sci USA. 98:2001;15342-15347.
21. ••].
22. ••].
23. Wu G.Y., Deisseroth K., Tsien R.W. Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci. 4:2001;151-158.
24. 2+/calmodulin translocation activated by mu-opioid (OP3) receptor. J Neurochem. 74:2000;1418-1425.
25. ••] demonstrated the crucial importance of the calmodulin-CaMKIV pathway to CREB in memory formation in the amygdala and hippocampus.
26. 2+-dependent nuclear accumulation of calmodulin. Proc Natl Acad Sci USA. 96:1999;6217-6222.
27. 2+-calmodulin signals in nucleus and cytosol. Curr Biol. 10:2000;86-94.
28. 2+/calmodulin kinase IV-deficient mice. J Neurosci 2000, 20:RC107:1-5.
29. ••].
30. 2+/calmodulin-dependent protein kinase type IV/Gr- deficient mice. J Neurosci. 20:2000;6459-6472.
31. 2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell. 87:1996;1203-1214.
32. 2+ stimulation of CREB- dependent transcription and ERK nuclear translocation. Neuron. 21:1998;869-883.
33. King D.P., Takahashi J.S. Molecular genetics of circadian rhythms in mammals. Annu Rev Neurosci. 23:2000;713-742.
34. Gau D., Lemberger T., von Gall C., Kretz O., Le Minh N., Gass P., Schmid W., Schibler U., Korf H.W., Schutz G. Phosphorylation of CREB Ser142 regulates light-induced phase shifts of the circadian clock. Neuron. 34:2002;245-253 This paper provided the first direct causal evidence linking CREB modulation to the important behavioral process of circadian rhythm entrainment. A crucial aspect of this link may lie in channel biophysics. Luckman et al. [36], Mermelstein et al. [39] and Deisseroth et al. [14] demonstrated that in hypothalamic and hippocampal neurons, nuclear signaling can filter out action potentials and respond selectively to synaptic potentials. A biophysical explanation was provided [39] linked to the activation gating kinetics of L-type calcium channels, a property that may be crucial in the behavioral roles of CREB (Figure 2).
35. Schurov I.L., Hepworth T.J., Hastings M.H. Dopaminergic signalling in the rodent neonatal suprachiasmatic nucleus identifies a role for protein kinase A and mitogen-activated protein kinase in circadian entrainment. Eur J Neurosci. 15:2002;223-232.
36. Luckman S.M., Dyball R.E., Leng G. Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. J Neurosci. 14:1994;4825-4830.
37. Chalazonitis A., Zigmond R.E. Effects of synaptic and antidromic stimulation on tyrosine hydroxylase activity in the rat superior cervical ganglion. J Physiol. 300:1980;525-538.
38. Brosenitsch T.A., Salgado-Commissariat D., Kunze D.L., Katz D.M. A role for L-type calcium channels in developmental regulation of transmitter phenotype in primary sensory neurons. J Neurosci. 18:1998;1047-1055.
39. Mermelstein P.G., Bito H., Deisseroth K., Tsien R.W. Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials. J Neurosci. 20:2000;266-273.
40. Akiyama M., Minami Y., Nakajima T., Moriya T., Shibata S. Calcium and pituitary adenylate cyclase-activating polypeptide induced expression of circadian clock gene mPer1 in the mouse cerebellar granule cell culture. J Neurochem. 78:2001;499-508.
41. Obrietan K., Impey S., Smith D., Athos J., Storm D.R. Circadian regulation of cAMP response element-mediated gene expression in the suprachiasmatic nuclei. J Biol Chem. 274:1999;17748-17756.
42. Travnickova-Bendova Z., Cermakian N., Reppert S.M., Sassone-Corsi P. Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc Natl Acad Sci USA. 99:2002;7728-7733.
43. Deisseroth K., Tsien R.W. Dynamic multiphosphorylation passwords for activity-dependent gene expression. Neuron. 34:2002;179-182.
44. Dudek S.M., Fields R.D. Somatic action potentials are sufficient for late-phase LTP-related cell signaling. Proc Natl Acad Sci USA. 99:2002;3962-3967.
45. Liu Z., Otsu Y., Murphy T.H. Analysis of the preference of the L-type VSCCs for different firing patterns in HEK cells and hippocampal neurons. Soc Neurosci Abstr. 707:1999;17.
46. Schafe G.E., Nader K., Blair H.T., LeDoux J.E. Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci. 24:2001;540-546.
47. Milner B., Squire L.R., Kandel E.R. Cognitive neuroscience and the study of memory. Neuron. 20:1998;445-468.
48. Impey S., Smith D.M., Obrietan K., Donahue R., Wade C., Storm D.R. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci. 1:1998;595-601.
49. Bourtchuladze R., Frenguelli B., Blendy J., Cioffi D., Schutz G., Silva A.J. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell. 79:1994;59-68.
50. •], demonstrates the importance of CREB in fear memory formation in the amygdala and the hippocampus, as well as the use of spaced training protocols to overcome insufficient CREB activation and lead to robust memory formation in both structures.
51. Kogan J.H., Frankland P.W., Blendy J.A., Coblentz J., Marowitz Z., Schutz G., Silva A.J. Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol. 7:1997;1-11.
52. •].
53. Bauer E.P., Schafe G.E., LeDoux J.E. NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci. 22:2002;5239-5249.
54. Weisskopf M.G., Bauer E.P., LeDoux J.E. L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. J Neurosci. 19:1999;10512-10519.
55. Vendrell M., Pujol M.J., Tusell J.M., Serratosa J. Effect of different convulsants on calmodulin levels and proto-oncogene c-fos expression in the central nervous system. Brain Res Mol Brain Res. 14:1992;285-292.
56. Milikan J.M., Bolsover S.R. Use of fluorescently labelled calmodulins as tools to measure subcellular calmodulin activation in living dorsal root ganglion cells. Pflugers Arch. 439:2000;394-400.
57. 2+-regulated dynamic compartmentalization of calmodulin in living smooth muscle cells. J Biol Chem. 270:1995;21532-21538.
58. Craske M., Takeo T., Gerasimenko O., Vaillant C., Torok K., Petersen O.H., Tepikin A.V. Hormone-induced secretory and nuclear translocation of calmodulin: oscillations of calmodulin concentration with the nucleus as an integrator. Proc Natl Acad Sci USA. 96:1999;4426-4431.
59. Sala C., Rudolph-Correia S., Sheng M. Developmentally regulated NMDA receptor-dependent dephosphorylation of cAMP response element-binding protein (CREB) in hippocampal neurons. J Neurosci. 20:2000;3529-3536.
60. 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.
61. Schafe G.E., Atkins C.M., Swank M.W., Bauer E.P., Sweatt J.D., LeDoux J.E. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J Neurosci. 20:2000;8177-8187.
62. Adams J.P., Sweatt J.D. Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu Rev Pharmacol Toxicol. 42:2002;135-163.
63. Liu F., Graybiel A.M. Activity-regulated phosphorylation of cAMP response element binding protein in the developing striatum: implications for patterning the neurochemical phenotypes of striatal compartments. Dev Neurosci. 20:1998;229-236.
64. •], a behavioral outcome that had been predicted earlier based on the potentiating effects of calcineurin inhibition on CREB function [31,63].
65. •].
66. Mantamadiotis T., Lemberger T., Bleckmann S.C., Kern H., Kretz O., Martin Villalba A., Tronche F., Kellendonk C., Gau D., Kapfhammer J.et al. Disruption of CREB function in brain leads to neurodegeneration. Nat Genet. 31:2002;47-54.
67. See V., Boutillier A.L., Bito H., Loeffler J.P. Calcium/calmodulin-dependent protein kinase type IV (CaMKIV) inhibits apoptosis induced by potassium deprivation in cerebellar granule neurons. FASEB J. 15:2001;134-144.
68. Bonni A., Brunet A., West A.E., Datta S.R., Takasu M.A., Greenberg M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science. 286:1999;1358-1362.
69. Shieh P.B., Hu S.C., Bobb K., Timmusk T., Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron. 20:1998;727-740.
70. Hardingham G.E., Bading H. Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated. Biochim Biophys Acta. 1600:2002;148-153.
71. Hardingham G.E., Fukunaga Y., Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci. 5:2002;405-414.
72. + efflux and neuronal apoptosis. Science. 284:1999;336-339.
73. Vyas S., Biguet N.F., Michel P.P., Monaco L., Foulkes N.S., Evan G.I., Sassone-Corsi P., Agid Y. Molecular mechanisms of neuronal cell death: implications for nuclear factors responding to cAMP and phorbol esters. Mol Cell Neurosci. 21:2002;1-14.
74. McKinsey T.A., Zhang C.L., Olson E.N. MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci. 27:2002;40-47.
75. Okamoto S., Li Z., Ju C., Scholzke M.N., Mathews E., Cui J., Salvesen G.S., Bossy-Wetzel E., Lipton S.A. Dominant-interfering forms of MEF2 generated by caspase cleavage contribute to NMDA-induced neuronal apoptosis. Proc Natl Acad Sci USA. 99:2002;3974-3979.
76. Mao Z., Bonni A., Xia F., Nadal-Vicens M., Greenberg M.E. Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science. 286:1999;785-790.
77. Li M., Linseman D.A., Allen M.P., Meintzer M.K., Wang X., Laessig T., Wierman M.E., Heidenreich K.A. Myocyte enhancer factor 2A and 2D undergo phosphorylation and caspase- mediated degradation during apoptosis of rat cerebellar granule neurons. J Neurosci. 21:2001;6544-6552.
78. Mattson M.P., Culmsee C., Yu Z., Camandola S. Roles of nuclear factor kappaB in neuronal survival and plasticity. J Neurochem. 74:2000;443-456.
79. Vermeulen L., De Wilde G., Notebaert S., Vanden Berghe W., Haegeman G. Regulation of the transcriptional activity of the nuclear factor-kappaB p65 subunit. Biochem Pharmacol. 64:2002;963-970.
80. 2+-dependent gene expression mediated by MEF2 transcription factors. J Biol Chem. 275:2000;197-209.
81. Groth R.D., Mermelstein P.G. Induction of NFAT-dependent transcription underlies BDNF-induced synaptic plasticity in hippocampal neurons. Soc Neurosci Abstr. 151:2002;15.
82. Inoue T., Kato K., Kohda K., Mikoshiba K. Type 1 inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J Neurosci. 18:1998;5366-5373.
83. Poo M.M. Neurotrophins as synaptic modulators. Nat Rev Neurosci. 2:2001;24-32.
84. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., Zaitsev E., Gold B., Goldman D., Dean M.et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell. 112:2003;257-269.