Genetic enhancement of trace fear memory and cingulate potentiation in mice overexpressing Ca2+/calmodulin-dependent protein kinase IV

European Journal of Neuroscience

Volumn 27, Issue 8, 2008, Pages 1923-1932

  Wu, Long Jun ^a   Zhang, Xue Han ^a,b   Fukushima, Hotaka ^c   Zhang, Fuxing ^a   Wang, Hansen ^a   Toyoda, Hiroki ^a   Li, Bao Ming ^b   Kida, Satoshi ^c   Zhuo, Min ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b FUDAN UNIVERSITY   (China)

^c TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

Author keywords

Anterior cingulate cortex; CaMKIV; Long term potentiation; Trace fear memory

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE (CALCIUM,CALMODULIN) IV; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CINGULATE GYRUS; CONTROLLED STUDY; FEAR; GENE CONTROL; GENETIC ENHANCEMENT; IMMUNOHISTOCHEMISTRY; LEARNING; LONG TERM POTENTIATION; MEMORY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OPEN FIELD BEHAVIOR; PATCH CLAMP; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; STATISTICAL ANALYSIS; SYNAPTIC TRANSMISSION; TAIL FLICK TEST; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; CEREBRAL CORTEX; CONDITIONING, CLASSICAL; FEAR; GENETIC ENHANCEMENT; IMMUNOHISTOCHEMISTRY; LONG-TERM POTENTIATION; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; SYNAPTIC TRANSMISSION;

EID: 42049086326     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06183.x     Document Type: Article

References (40)

1. Ahn, S., Ginty, D.D. Linden, D.J. (1999) A late phase of cerebellar long-term depression requires activation of CaMKIV and CREB. Neuron, 23, 559 568.
2. 2+/calmodulin-dependent protein kinase IV and calcium signaling. Biometals, 11, 331 343.
3. Barco, A., Alarcon, J.M. Kandel, E.R. (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell, 108, 689 703.
4. Bito, H., Deisseroth, K. Tsien, R.W. (1996) CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell, 87, 1203 1214.
5. 2+/calmodulin kinase kinase alpha-deficient mice. Mol. Cell Biol., 26, 9105 9115.
6. Boyden, E.S., Katoh, A., Pyle, J.L., Chatila, T.A., Tsien, R.W. Raymond, J.L. (2006) Selective engagement of plasticity mechanisms for motor memory storage. Neuron, 51, 823 834.
7. Frankland, P.W., Bontempi, B., Talton, L.E., Kaczmarek, L. Silva, A.J. (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science, 304, 881 883.
8. Han, C.J., O'Tuathaigh, C.M., van Trigt, L., Quinn, J.J., Fanselow, M.S., Mongeau, R., Koch, C. Anderson, D.J. (2003) Trace but not delay fear conditioning requires attention and the anterior cingulate cortex. Proc. Natl Acad. Sci. USA, 100, 13087 13092.
9. 2+/calmodulin-dependent protein kinase type IV/Gr-deficient mice. J. Neurosci., 20, 6459 6472.
10. Hosoda, H., Motohashi, J., Kato, H., Masushige, S. Kida, S. (2004) A BMAL1 mutant with arginine 91 substituted with alanine acts as a dominant negative inhibitor. Gene, 338, 235 241.
11. Huerta, P.T., Sun, L.D., Wilson, M.A. Tonegawa, S. (2000) Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron, 25, 473 480.
12. Kang, H., Sun, L.D., Atkins, C.M., Soderling, T.R., Wilson, M.A. Tonegawa, S. (2001) An important role of neural activity-dependent CaMKIV signaling in the consolidation of long-term memory. Cell, 106, 771 783.
13. Kasahara, J., Fukunaga, K. Miyamoto, E. (2001) Activation of calcium/calmodulin-dependent protein kinase IV in long term potentiation in the rat hippocampal CA1 region. J. Biol. Chem., 276, 24044 24050.
14. Kida, S., Josselyn, S.A., de Ortiz, S.P., Kogan, J.H., Chevere, I., Masushige, S. Silva, A.J. (2002) CREB required for the stability of new and reactivated fear memories. Nat. Neurosci., 5, 348 355.
15. Ko, S.W., Chatila, T. Zhuo, M. (2005) Contribution of CaMKIV to injury and fear-induced ultrasonic vocalizations in adult mice. Mol. Pain, 1, 10.
16. Liauw, J., Wu, L.J. Zhuo, M. (2005) Calcium-stimulated adenylyl cyclases required for long-term potentiation in the anterior cingulate cortex. J. Neurophysiol., 94, 878 882.
17. Marie, H., Morishita, W., Yu, X., Calakos, N. Malenka, R.C. (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron, 45, 741 752.
18. Maviel, T., Durkin, T.P., Menzaghi, F. Bontempi, B. (2004) Sites of neocortical reorganization critical for remote spatial memory. Science, 305, 96 99.
19. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D. Kandel, E.R. (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science, 274, 1678 1683.
20. 2+/calmodulin- dependent kinase IV/Gr-dependent phosphorylation of oncoprotein 18. Mol. Cell Biol., 17, 3459 3467.
21. 2+/calmodulin kinase kinase alpha is dispensable for brain development but is required for distinct memories in male, though not in female, mice. Mol. Cell Biol., 26, 9094 9104.
22. 2+/calmodulin kinase kinase beta affects the formation of some, but not all, types of hippocampus-dependent long-term memory. J. Neurosci., 23, 9752 9760.
23. Redmond, L., Kashani, A.H. Ghosh, A. (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron, 34, 999 1010.
24. 2+/calmodulin kinase IV-deficient mice. J Neurosci, 20, RC107.
25. Shaywitz, A.J. Greenberg, M.E. (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem., 68, 821 861.
26. Shum, F.W., Ko, S.W., Lee, Y.S., Kaang, B.K. Zhuo, M. (2005) Genetic alteration of anxiety and stress-like behavior in mice lacking CaMKIV. Mol. Pain, 1, 22.
27. Shumyatsky, G.P., Malleret, G., Shin, R.M., Takizawa, S., Tully, K., Tsvetkov, E., Zakharenko, S.S., Joseph, J., Vronskaya, S., Yin, D., Schubart, U.K., Kandel, E.R. Bolshakov, V.Y. (2005) Stathmin, a gene enriched in the amygdala, controls both learned and innate fear. Cell, 123, 697 709.
28. Soderling, T.R. (1999) The Ca-calmodulin-dependent protein kinase cascade. Trends Biochem. Sci., 24, 232 236.
29. Toyoda, H., Wu, L.J., Zhao, M.G., Xu, H. Zhuo, M. (2007) Time-dependent postsynaptic AMPA GluR1 receptor recruitment in the cingulate synaptic potentiation. Dev. Neurobiol., 67, 498 509.
30. Wang, H., Gong, B., Vadakkan, K.I., Toyoda, H., Kaang, B.K. Zhuo, M. (2007) Genetic evidence for adenylyl cyclase 1 as a target for preventing neuronal excitotoxicity mediated by N-methyl-D-aspartate receptors. J. Biol. Chem., 282, 1507 1517.
31. Wang, C.C. Shyu, B.C. (2004) Differential projections from the mediodorsal and centrolateral thalamic nuclei to the frontal cortex in rats. Brain Res., 995, 226 235.
32. Wei, F., Qiu, C.S., Liauw, J., Robinson, D.A., Ho, N., Chatila, T. Zhuo, M. (2002) Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat. Neurosci., 5, 573 579.
33. Wei, F. Zhuo, M. (2001) Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat. J. Physiol., 532, 823 833.
34. Wu, L.J., Toyoda, H., Zhao, M.G., Lee, Y.S., Tang, J., Ko, S.W., Jia, Y.H., Shum, F.W., Zerbinatti, C.V., Bu, G., Wei, F., Xu, T.L., Muglia, L.J., Chen, Z.F., Auberson, Y.P., Kaang, B.K. Zhuo, M. (2005a) Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. J. Neurosci., 25, 11107 11116.
35. Wu, L.J., Zhao, M.G., Toyoda, H., Ko, S.W. Zhuo, M. (2005b) Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J. Neurophysiol., 94, 1805 1813.
36. Zhao, M.G., Ko, S.W., Wu, L.J., Toyoda, H., Xu, H., Quan, J., Li, J., Jia, Y., Ren, M., Xu, Z.C. Zhuo, M. (2006) Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. J. Neurosci., 26, 8923 8930.
37. Zhao, M.G., Toyoda, H., Ko, S.W., Ding, H.K., Wu, L.J. Zhuo, M. (2005a) Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J. Neurosci., 25, 7385 7392.
38. Zhao, M.G., Toyoda, H., Lee, Y.S., Wu, L.J., Ko, S.W., Zhang, X.H., Jia, Y., Shum, F., Xu, H., Li, B.M., Kaang, B.K. Zhuo, M. (2005b) Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron, 47, 859 872.
39. Zhuo, M. (2006) Molecular mechanisms of pain in the anterior cingulate cortex. J. Neurosci. Res., 84, 927 933.
40. Zhuo, M. (2007) Neuronal mechanism for neuropathic pain. Mol. Pain, 3, 14.