The role of hippocampal signaling cascades in consolidation of fear memory

Behavioural Brain Research

Volumn 149, Issue 1, 2004, Pages 17-31

  Ahi, Janak ^a,b   Radulovic, Jelena ^a   Spiess, Joachim ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b DR H S GOUR UNIVERSITY   (India)

Author keywords

CaMK II; Fear conditioning; Mek 1 2; pCREB; pElk 1; pErk 1 2; PKA; PKC; pp90Rsk 1

Indexed keywords

BRAIN ENZYME; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PHOSPHOTRANSFERASE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE C; TRANSCRIPTION FACTOR ELK 1;

ANIMAL EXPERIMENT; ARTICLE; CONDITIONING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEAR; FREEZING; HIPPOCAMPUS; MALE; MEMORY CONSOLIDATION; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; RIBOSOME; SHOCK; SIGNAL TRANSDUCTION; STIMULUS; TRAINING;

EID: 0347931766     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(03)00207-9     Document Type: Article

References (59)

1. Abel T., Ngyen P.V., Barad M., Deuel T.A., Kandel E.R., Bourtchouladze R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell. 88:1997;615-626.
2. Abeliovich A., Paylor R., Chen C., Kim J.J., Wehner J.M., Tonegawa S. PKC gamma mutant mice exhibit mild deficits in spatial and contextual learning. Cell. 75:1993;1263-1271.
3. Atkins C.M., Selcher J.C., Petraitis J.J., Trzaskos J.M., Sweatt J.D. The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1:1998;602-609.
4. Bach M.E., Hawkins R.D., Osman M., Kandel E.R., Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell. 81:1995;905-915.
5. Barros D.M., Izquierdo L.A., Sant'Anna M.K., Quevedo J., Medina J.H., McGaugh J.L.et al. Stimulators of the cAMP cascade reverse amnesia induced by intra-amygdala but not intrahippocampal KN-62 administration. Neurobiol. Learn. Mem. 71:1999;94-103.
6. Berman D., Hazvi S., Rosenblum K., Seger R., Dudai Y. Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J. Neurosci. 18:1998;10037-10044.
7. Blank T., Nijholt I., Eckart K., Spiess J. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J. Neurosci. 22:2002;3788-3794.
8. Blum S., Moore A.N., Adams F., Dash P.K. A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. J. Neurosci. 19:1999;3535-3544.
9. 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.
10. Bourtchouladze R., Abel T., Berman N., Gordon R., Lapidus K., Kandel E.R. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn. Mem. 5:1998;365-374.
11. Cammarota M., Bevilaqua L.R., Ardenghi P., Paratcha G., Levi de Stein M., Izquierdo I.et al. Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: abolition by NMDA receptor blockade. Brain Res. Mol. Brain Res. 76:2000;36-46.
12. Chen R.H., Chung J., Blenis J. Regulation of pp90rsk phosphorylation and S6 phosphotransferase activity in Swiss 3T3 cells by growth factor-, phorbolester-, and cyclic AMP-mediated signal transduction. Mol. Cell. Biol. 11:1991;1861-1867.
13. Chen R.H., Sarnecki C., Blenis J. Nuclear localization and regulation of erk- and rsk-encoded protein kinases. Mol. Cell. Biol. 12:1992;915-927.
14. Chen R.H., Tung R., Abate C., Blenis J. Cytoplasmic to nuclear signal transduction by mitogen-activated protein kinase and 90. kDa ribosomal S6 kinase Biochem. Soc. Trans. 21:1993;895-900.
15. Choe E.S., McGinty J.F. N-Methyl-D-aspartate receptors and p38 mitogen-activated protein kinase are required for cAMP-dependent cyclase response element binding protein and Elk-1 phosphorylation in the striatum. Neuroscience. 101:2000;607-617.
16. Crow T., Xue-Bian J.J., Siddiqi V., Kang Y., Neary J.T. Phosphorylation of mitogen-activated protein kinase by one-trial and multi-trial classical conditioning. J. Neurosci. 18:1998;3480-3487.
17. Davis H.P., Squire L.R. Protein synthesis and memory. A review. Psychol. Bull. 96:1984;518-559.
18. 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.
19. Flexner L.B., Flexner J.B., Stellar E. Memory and cerebral protein synthesis in mice is affected by graded amounts of puromycin. Exp. Neurol. 13:1965;264-272.
20. Frankland P.W., O'Brien C., Ohno M., Kirkwood A., Silva A.J. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature. 411:2001;309-313.
21. Franklin KBJ, Paxinos G, editors. The mouse brain in stereotaxic coordinates. San Diego: Academic Press; 1997.
22. Frodin M., Gammeloft S. Role and regulation of 90. kDa ribosomal S6 kinase (RSK) in signal transduction Mol. Cell. Endocrinol. 151:1999;65-77.
23. Goosens K.A., Holt W., Maren S. A role for amygdaloid PKA and PKC in the acquisition of long-term conditional fear memories in rats. Behav. Brain Res. 114:2000;145-152.
24. Grewal S.S., York R.D., Stork P.J. Extracellular-signal-related kinases. Curr. Opin. Neurobiol. 9:1999;544-553.
25. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron. 21:1998;869-883.
26. Kaminska B., Kaczmarek L., Zangenehpour S., Chaudhuri A. Rapid phosphorylation of Elk-1 transcription factor and activation of MAP kinase signal transduction pathways in response to visual stimulation. Mol. Cell. Neurosci. 13:1999;405-414.
27. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science. 256:1992;675-677.
28. Micheau J., Riedel G. Protein kinases: which one is the memory molecule? Cell. Mol. Life Sci. 55:1999;534-548.
29. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106:1992;274-285.
30. Platenik J., Kuramoto N., Yoneda Y. Molecular mechanisms associated with long-term consolidation of the NMDA signals. Life Sci. 67:2000;335-364.
31. Radulovic J., Kammermeier J., Spiess J. Generalization of fear responses in C57BL/6N mice subjected to one-trial foreground contextual fear conditioning. Behav. Brain Res. 95:1998;179-189.
32. Radulovic J., Sydow S., Spiess J. Characterization of native corticotropin-releasing factor receptor type 1 (CRFR1) in the rat and mouse central nervous system. J. Neurosci. Res. 54:1998;507-521.
33. Radulovic J., Kammermeier J., Spiess J. Relationship between fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J. Neurosci. 18:1998;7452-7461.
34. Radulovic J., Ruhmann A., Liepold T., Spiess J. Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J. Neurosci. 19:1999;5016-5025.
35. Rao V.N., Reddy E.S. Elk-1 proteins are phosphoproteins and activators of mitogen-activated protein kinase. Cancer Res. 53:1993;3449-3454.
36. Rao V.N., Reddy E.S. Elk-1 proteins interact with MAP kinases. Oncogene. 9:1994;1855-1860.
37. 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.
38. Rosenzweig M.R., Bennett E., Colombo P.J., Lee D.W., Serrano P.A. Short-term, intermediate-term, and long-term memories. Behav. Brain Res. 57:1993;193-198.
39. Sananbenesi F., Fischer A., Schrick C., Spiess J., Radulovic J. Phosphorylation of hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during contextual fear conditioning: interactions between Erk-1/2 and Elk-1. Mol. Cell. Neurosci. 21:2002;463-476.
40. Schafe G.E., Nadel N.V., Sullivan G.M., Harris A., LeDoux J.E. Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn. Mem. 6:1999;97-110.
41. 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.
42. Schafe G.E., LeDoux J.E. Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci. 20:2000;RC96.
43. Selcher J.C., Weeber E.J., Christian J., Nekrasova T., Landreth G.E., Sweatt J.D. A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn. Mem. 10:2003;26-39.
44. Sgambato V., Pages C., Rogard M., Besson M.J., Caboche J. Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J. Neurosci. 18:1998;8814-8825.
45. Silva A.J., Kogan J.H., Frankland P.W., Kida S. CREB and memory. Annu. Rev. Neurosci. 21:1998;127-148.
46. Snabaitis A.K., Yokoyama H., Avkiran M. Roles of mitogen-activated protein kinases and protein kinase C in alpha(1A)-adrenoceptor-mediated stimulation of the sarcolemmal Na(+)-H(+) exchanger. Circ. Res. 86:2000;214-220.
47. Soderling T. Calcium/calmodulin-dependent protein kinase II: role in learning and memory. Mol. Cell. Biochem. 127/128:1993;93-101.
48. Soderling T.R., Derkach V.A. Postsynaptic protein phosphorylation and LTP. Trends Neurosci. 23:2000;75-80.
49. Stanciu M., Radulovic J., Spiess J. Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: relationship to FOS production. Mol. Brain Res. 94:2001;15-24.
50. Stiedl O., Spiess J. Effect of tone-dependent fear conditioning on heart rate and behavior of C57BL/6N mice. Behav. Neurosci. 111:1997;703-711.
51. 2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 8:1994;2527-2539.
52. Swank M.W., Sweatt J.D. Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. J. Neurosci. 21:2001;3383-3391.
53. Sweatt J.D. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76:2001;1-10.
54. Treisman R. Journey to the surface of the cell: fos regulation and the SRE. EMBO J. 14:1995;4905-4913.
55. Treisman R. Regulation of transcription by MAP kinase cascade. Curr. Opin. Cell Biol. 8:1996;205-215.
56. Vanhoutte P., Barnier J.V., Guibert B., Pages C., Besson M.J., Hipskind R.A.et al. Glutamate induces phosphorylation of Elk-1 and CREB, along with c-fos activation, via an extracellular signal-regulated kinase-dependent pathway in brain slices. Mol. Cell. Biol. 19:1999;136-146.
57. Weeber E.J., Atkins C.M., Selcher J.C., Varga A.W., Mirnikjoo B., Paylor R.et al. A role for the beta isoform of protein kinase C in fear conditioning. J. Neurosci. 20:2000;5906-5914.
58. Wehner J.M., Sleight S., Upchurch M. Hippocampal protein kinase C activity is reduced in poor spatial learners. Brain Res. 523:1990;181-187.
59. Xing J., Ginty D.D., Greenberg M.E. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science. 273:1996;959-963.