Hippocampal CARP over-expression solidifies consolidation of contextual fear memories

Physiology and Behavior

Volumn 102, Issue 3-4, 2011, Pages 323-331

  Schenk, Geert J ^a   Vreugdenhil, Erno ^a   Hubens, Chantal J Y ^a   Veldhuisen, Barbera ^a   de Kloet, E Ron ^a   Oitzl, Melly S ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

CARP; DCLK; DCX; Fear conditioning; In situ hybridization; Memory; Transgenic mice

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE;

ADAPTIVE BEHAVIOR; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; HIPPOCAMPUS; MALE; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE; WILD TYPE;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CONDITIONING, CLASSICAL; CORTICOSTERONE; FEAR; HIPPOCAMPUS; MEMORY; MICE; MICE, TRANSGENIC; PAIN PERCEPTION; PHOSPHOPROTEINS; RADIOIMMUNOASSAY;

EID: 78650413372     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.11.024     Document Type: Article

References (73)

1. Burgess H.A., Reiner O. Alternative splice variants of doublecortin-like kinase are differentially expressed and have different kinase activities. J Biol Chem 2002, 277(20):17,696-17,705.
2. Friocourt G., Koulakoff A., Chafey P., Boucher D., Fauchereau F., Chelly J., et al. Doublecortin functions at the extremities of growing neuronal processes. Cereb Cortex 2003, 13(6):620-626.
3. Vreugdenhil E., Engels B., Middelburg R., van Koningsbruggen S., Knol J., Veldhuisen B., et al. Multiple transcripts generated by the DCAMKL gene are expressed in the rat hippocampus. Brain Res Mol Brain Res 2001, 94(1-2):67-74.
4. Vreugdenhil E., Kolk S.M., Boekhoorn K., Fitzsimons C.P., Schaaf M., Schouten T., et al. Doublecortin-like, a microtubule-associated protein expressed in radial glia, is crucial for neuronal precursor division and radial process stability. Eur J Neurosci 2007, 25(3):635-648.
5. Koizumi H., Tanaka T., Gleeson J.G. Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 2006, 49(1):55-66.
6. Deuel T.A., Liu J.S., Corbo J.C., Yoo S.Y., Rorke-Adams L.B., Walsh C.A. Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 2006, 49(1):41-53.
7. Tanaka T., Koizumi H., Gleeson J.G. The doublecortin and doublecortin-like kinase 1 genes cooperate in murine hippocampal development. Cereb Cortex 2006, 16(Suppl 1):i69-i73.
8. Friocourt G., Liu J.S., Antypa M., Rakic S., Walsh C.A., Parnavelas J.G. Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci 2007, 27(14):3875-3883.
9. Vreugdenhil E., Datson N., Engels B., de Jong J., van Koningsbruggen S., Schaaf M., et al. Kainate-elicited seizures induce mRNA encoding a CaMK-related peptide: a putative modulator of kinase activity in rat hippocampus. J Neurobiol 1999, 39(1):41-50.
10. Berke J.D., Sgambato V., Zhu P.P., Lavoie B., Vincent M., Krause M., et al. Dopamine and glutamate induce distinct striatal splice forms of Ania-6, an RNA polymerase II-associated cyclin. Neuron 2001, 32(2):277-287.
11. Schenk G.J., Engels B., Zhang Y.P., Fitzsimons C.P., Schouten T., Kruidering M., et al. A potential role for calcium/calmodulin-dependent protein kinase-related peptide in neuronal apoptosis: in vivo and in vitro evidence. Eur J Neurosci 2007, 26(12):3411-3420.
12. Wibrand K., Messaoudi E., Havik B., Steenslid V., Lovlie R., Steen V.M., et al. Identification of genes co-upregulated with Arc during BDNF-induced long-term potentiation in adult rat dentate gyrus in vivo. Eur J Neurosci 2006, 23(6):1501-1511.
13. Kawaai K., Tominaga-Yoshino K., Urakubo T., Taniguchi N., Kondoh Y., Tashiro H., et al. Analysis of gene expression changes associated with long-lasting synaptic enhancement in hippocampal slice cultures after repetitive exposures to glutamate. J Neurosci Res 2010, 88(13):2911-2922.
14. Schenk G.J., Werkman T., Wadman W., Veldhuisen B., Dijkmans T.F., Blaas E., et al. Over-expression of the DCLK gene transcript CARP decreases CA3/CA1 network excitability. Brain Res 2010, 1352:21-34.
15. Maren S. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 2001, 24:897-931.
16. Ji J., Maren S. Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 2007, 17(9):749-758.
17. Ji J., Maren S. Lesions of the entorhinal cortex or fornix disrupt the context-dependence of fear extinction in rats. Behav Brain Res 2008, 194(2):201-206.
18. Vidal M., Morris R., Grosveld F., Spanopoulou E. Tissue-specific control elements of the Thy-1 gene. EMBO J 1990, 9(3):833-840.
19. Hirrlinger P.G., Scheller A., Braun C., Quintela-Schneider M., Fuss B., Hirrlinger J., et al. Expression of reef coral fluorescent proteins in the central nervous system of transgenic mice. Mol Cell Neurosci 2005, 30(3):291-303.
20. Moechars D., Lorent K., De Strooper B., Dewachter I., Van Leuven F. Expression in brain of amyloid precursor protein mutated in the alpha-secretase site causes disturbed behavior, neuronal degeneration and premature death in transgenic mice. EMBO J 1996, 15(6):1265-1274.
21. Schenk G.J., Veldhuisen B., Wedemeier O., McGown C.C., Schouten T.G., Oitzl M., et al. Over-expression of deltaC-DCLK-short in mouse brain results in a more anxious behavioral phenotype. Physiol Behav 2010, 101(4):541-548.
22. Meijer O.C., Steenbergen P.J., De Kloet E.R. Differential expression and regional distribution of steroid receptor coactivators SRC-1 and SRC-2 in brain and pituitary. Endocrinology 2000, 141(6):2192-2199.
23. Brinks V., de Kloet E.R., Oitzl M.S. Strain specific fear behaviour and glucocorticoid response to aversive events: modelling PTSD in mice. Prog Brain Res 2008, 167:257-261.
24. Bilsky E.J., Inturrisi C.E., Sadee W., Hruby V.J., Porreca F. Competitive and non-competitive NMDA antagonists block the development of antinociceptive tolerance to morphine, but not to selective mu or delta opioid agonists in mice. Pain 1996, 68(2-3):229-237.
25. Dalm S., Enthoven L., Meijer O.C., van der Mark M.H., Karssen A.M., de Kloet E.R., et al. Age-related changes in hypothalamic-pituitary-adrenal axis activity of male C57BL/6J mice. Neuroendocrinology 2005, 81(6):372-380.
26. Franklin K.B.J.a.P.G. The mouse brain in stereotaxic coordinates 1997, Academic Press.
27. Cordero M.I., Kruyt N.D., Merino J.J., Sandi C. Glucocorticoid involvement in memory formation in a rat model for traumatic memory. Stress 2002, 5(1):73-79.
28. Cordero M.I., Venero C., Kruyt N.D., Sandi C. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm Behav 2003, 44(4):338-345.
29. Cai W.H., Blundell J., Han J., Greene R.W., Powell C.M. Postreactivation glucocorticoids impair recall of established fear memory. J Neurosci 2006, 26(37):9560-9566.
30. McGaugh J.L., Roozendaal B. Drug enhancement of memory consolidation: historical perspective and neurobiological implications. Psychopharmacology (Berl) 2009, 202(1-3):3-14.
31. Datson N.A., van der Perk J., de Kloet E.R., Vreugdenhil E. Identification of corticosteroid-responsive genes in rat hippocampus using serial analysis of gene expression. Eur J Neurosci 2001, 14(4):675-689.
32. Alfonso J., Aguero F., Sanchez D.O., Flugge G., Fuchs E., Frasch A.C., et al. Gene expression analysis in the hippocampal formation of tree shrews chronically treated with cortisol. J Neurosci Res 2004, 78(5):702-710.
33. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48(2):175-187.
34. Rosen J.B., Donley M.P. Animal studies of amygdala function in fear and uncertainty: relevance to human research. Biol Psychol 2006, 73(1):49-60.
35. Herry C., Ciocchi S., Senn V., Demmou L., Muller C., Luthi A. Switching on and off fear by distinct neuronal circuits. Nature 2008, 454(7204):600-606.
36. Maren S., Holt W. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav Brain Res 2000, 110(1-2):97-108.
37. Sandi C., Cordero M.I., Ugolini A., Varea E., Caberlotto L., Large C.H. Chronic stress-induced alterations in amygdala responsiveness and behavior-modulation by trait anxiety and corticotropin-releasing factor systems. Eur J Neurosci 2008, 28(9):1836-1848.
38. Goosens K.A., Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn Mem 2001, 8(3):148-155.
39. Kim J.J., Jung M.W. Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 2006, 30(2):188-202.
40. Glavan G., Sket D., Zivin M. Modulation of neuroleptic activity of 9, 10-didehydro-N-methyl-(2-propynyl)-6-methyl-8-aminomethylergoline bimaleinate (LEK-8829) by D1 intrinsic activity in hemi-parkinsonian rats. Mol Pharmacol 2002, 61(2):360-368.
41. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev 1998, 19(3):269-301.
42. Brinks V., van der Mark M.H., de Kloet E.R., Oitzl M.S. Differential MR/GR activation in mice results in emotional states beneficial or impairing for cognition. Neural Plast 2007, 2007:90,163.
43. Brown-Croyts L.M., Caton P.W., Radecki D.T., McPherson S.L. Phenobarbital pre-treatment prevents kainic acid-induced impairments in acquisition learning. Life Sci 2000, 67(6):643-650.
44. Ben-Ari Y. Cell death and synaptic reorganizations produced by seizures. Epilepsia 2001, 42(Suppl 3):5-7.
45. Jessberger S., Nakashima K., Clemenson G.D., Mejia E., Mathews E., Ure K., et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 2007, 27(22):5967-5975.
46. Parent J.M., Lowenstein D.H. Seizure-induced neurogenesis: are more new neurons good for an adult brain?. Prog Brain Res 2002, 135:121-131.
47. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361(6407):31-39.
48. Lynch M.A. Long-term potentiation and memory. Physiol Rev 2004, 84(1):87-136.
49. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256(5057):675-677.
50. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992, 106(2):274-285.
51. Li Z., Zhou Q., Li L., Mao R., Wang M., Peng W., et al. Effects of unconditioned and conditioned aversive stimuli in an intense fear conditioning paradigm on synaptic plasticity in the hippocampal CA1 area in vivo. Hippocampus 2005, 15(6):815-824.
52. Gruart A., Munoz M.D., Delgado-Garcia J.M. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 2006, 26(4):1077-1087.
53. Liu I.Y., Lyons W.E., Mamounas L.A., Thompson R.F. Brain-derived neurotrophic factor plays a critical role in contextual fear conditioning. J Neurosci 2004, 24(36):7958-7963.
54. Liu L., Zhang S., Zhu Y., Fu Q., Zhu Y., Gong Y., et al. Improved learning and memory of contextual fear conditioning and hippocampal CA1 long-term potentiation in histidine decarboxylase knock-out mice. Hippocampus 2007, 17(8):634-641.
55. Wu L.J., Ren M., Wang H., Kim S.S., Cao X., Zhuo M. Neurabin contributes to hippocampal long-term potentiation and contextual fear memory. PLoS ONE 2008, 3(1):e1407.
56. Krucker T., Siggins G.R., Halpain S. Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci USA 2000, 97(12):6856-6861.
57. Ressler K.J., Paschall G., Zhou X.L., Davis M. Regulation of synaptic plasticity genes during consolidation of fear conditioning. J Neurosci 2002, 22(18):7892-7902.
58. Meng Y., Zhang Y., Tregoubov V., Janus C., Cruz L., Jackson M., et al. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 2002, 35(1):121-133.
59. Fischer A., Sananbenesi F., Schrick C., Spiess J., Radulovic J. Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear. J Neurosci 2004, 24(8):1962-1966.
60. Rabenstein R.L., Addy N.A., Caldarone B.J., Asaka Y., Gruenbaum L.M., Peters L.L., et al. Impaired synaptic plasticity and learning in mice lacking beta-adducin, an actin-regulating protein. J Neurosci 2005, 25(8):2138-2145.
61. Dijkmans T.F., van Hooijdonk L.W., Schouten T.G., Kamphorst J.T., Fitzsimons C.P., Vreugdenhil E. Identification of new nerve growth factor-responsive immediate-early genes. Brain Res 2009, 1249:19-33.
62. Moeller M.L., Shi Y., Reichardt L.F., Ethell I.M. EphB receptors regulate dendritic spine morphogenesis through the recruitment/phosphorylation of focal adhesion kinase and RhoA activation. J Biol Chem 2006, 281(3):1587-1598.
63. Buday L., Wunderlich L., Tamas P. The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal 2002, 14(9):723-731.
64. Katz M.E., McCormick F. Signal transduction from multiple Ras effectors. Curr Opin Genet Dev 1997, 7(1):75-79.
65. Schafe G.E., Swank M.W., Rodrigues S.M., Debiec J., Doyere V. Phosphorylation of ERK/MAP kinase is required for long-term potentiation in anatomically restricted regions of the lateral amygdala in vivo. Learn Mem 2008, 15(2):55-62.
66. Herry C., Trifilieff P., Micheau J., Luthi A., Mons N. Extinction of auditory fear conditioning requires MAPK/ERK activation in the basolateral amygdala. Eur J Neurosci 2006, 24(1):261-269.
67. Trifilieff P., Herry C., Vanhoutte P., Caboche J., Desmedt A., Riedel G., et al. Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn Mem 2006, 13(3):349-358.
68. Chwang W.B., O'Riordan K.J., Levenson J.M., Sweatt J.D. ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learn Mem 2006, 13(3):322-328.
69. Lewis M.C., Gould T.J. Signal transduction mechanisms within the entorhinal cortex that support latent inhibition of cued fear conditioning. Neurobiol Learn Mem 2007, 88(3):359-368.
70. Sindreu C.B., Scheiner Z.S., Storm D.R. Ca2+-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 2007, 53(1):79-89.
71. 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 1998, 1(7):602-609.
72. 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 1999, 19(9):3535-3544.
73. Boekhoorn K., Sarabdjitsingh A., Kommerie H., de Punder K., Schouten T., Lucassen P.J., et al. Doublecortin (DCX) and doublecortin-like (DCL) are differentially expressed in the early but not late stages of murine neocortical development. J Comp Neurol 2008, 507(4):1639-1652.